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Published in: Documenta Ophthalmologica 3/2013

01-12-2013 | Original Research Article

Pattern electroretinogram in neuromyelitis optica and multiple sclerosis with or without optic neuritis and its correlation with FD-OCT and perimetry

Authors: Kenzo Hokazono, Ali S. Raza, Maria K. Oyamada, Donald C. Hood, Mário L. R. Monteiro

Published in: Documenta Ophthalmologica | Issue 3/2013

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Abstract

Purpose

To evaluate the ability of transient pattern electroretinogram (PERG) parameters to differentiate between eyes of patients with neuromyelitis optica (NMO), longitudinally extensive transverse myelitis (LETM), multiple sclerosis with optic neuritis (MS + ON), multiple sclerosis without optic neuritis (MS − ON), and controls, to compare PERG and OCT with regard to discrimination ability, and to assess the correlation between PERG, FD-OCT, and visual field measurements (VFs).

Methods

Visual field measurements and full-field stimulation PERGs based on both 48- and 14-min checks were obtained from patients with MS (n = 28), NMO (n = 20), LETM (n = 18), and controls (n = 26). In addition, FD-OCT peripapillary retinal nerve fiber layer (RNFL) and segmented macular layer measurements were obtained and their correlation coefficients were determined.

Results

Compared to controls, PERG amplitude measurements were significantly reduced in eyes with NMO and MS + ON, but not in eyes with LETM and MS − ON. PERG amplitudes were significantly smaller in NMO and MS + ON eyes than in MS − ON eyes. PERG and OCT performance was similar except in NMO eyes where macular thickness parameters were more efficient at detecting abnormalities. A significant correlation was found between N95 amplitude values and OCT-measured macular ganglion cell layer thickness, total retinal thickness, and temporal peripapillary RNFL thickness. PERG amplitude was also significantly associated with VF sensitivity loss. No statistically significant difference was observed with regard to the best-performing parameters of the two methods.

Conclusions

Pattern electroretinogram measurements were able to detect RNFL loss in MS + ON and NMO eyes, with a performance comparable to OCT. PERG amplitude measurements were reasonably well correlated with OCT-measured parameters.
Literature
1.
go back to reference Fernandes DB, Ramos Rde I, Falcochio C, Apóstolos-Pereira S, Callegaro D, Monteiro ML (2012) Comparison of visual acuity and automated perimetry findings in patients with neuromyelitis optica or multiple sclerosis after single or multiple attacks of optic neuritis. J Neuroophthalmol 32:102–106 Fernandes DB, Ramos Rde I, Falcochio C, Apóstolos-Pereira S, Callegaro D, Monteiro ML (2012) Comparison of visual acuity and automated perimetry findings in patients with neuromyelitis optica or multiple sclerosis after single or multiple attacks of optic neuritis. J Neuroophthalmol 32:102–106
2.
go back to reference Fazekas F, Barkhof F, Filippi M (1998) Unenhanced and enhanced magnetic resonance imaging in the diagnosis of multiple sclerosis. J Neurol Neurosurg Psychiatry 64(Suppl 1):S2–S5PubMed Fazekas F, Barkhof F, Filippi M (1998) Unenhanced and enhanced magnetic resonance imaging in the diagnosis of multiple sclerosis. J Neurol Neurosurg Psychiatry 64(Suppl 1):S2–S5PubMed
3.
go back to reference Monteiro ML, Fernandes DB, Apostolos-Pereira SL, Callegaro D (2012) Quantification of retinal neural loss in patients with neuromyelitis optica and multiple sclerosis with or without optic neuritis using Fourier-domain optical coherence tomography. Invest Ophthalmol Vis Sci 53:3959–3966CrossRefPubMed Monteiro ML, Fernandes DB, Apostolos-Pereira SL, Callegaro D (2012) Quantification of retinal neural loss in patients with neuromyelitis optica and multiple sclerosis with or without optic neuritis using Fourier-domain optical coherence tomography. Invest Ophthalmol Vis Sci 53:3959–3966CrossRefPubMed
4.
go back to reference Fernandes DB, Raza AS, Nogueira RG, Wang D, Callegaro D, Hood DC, Monteiro ML (2013) Evaluation of inner retinal layers in patients with multiple sclerosis or neuromyelitis optica using optical coherence tomography. Ophthalmology 120:387–394CrossRefPubMed Fernandes DB, Raza AS, Nogueira RG, Wang D, Callegaro D, Hood DC, Monteiro ML (2013) Evaluation of inner retinal layers in patients with multiple sclerosis or neuromyelitis optica using optical coherence tomography. Ophthalmology 120:387–394CrossRefPubMed
5.
go back to reference Henderson AP, Trip SA, Schlottmann PG, Altmann DR, Garway-Heath DF, Plant GT, Miller DH (2008) An investigation of the retinal nerve fibre layer in progressive multiple sclerosis using optical coherence tomography. Brain 131:277–287PubMed Henderson AP, Trip SA, Schlottmann PG, Altmann DR, Garway-Heath DF, Plant GT, Miller DH (2008) An investigation of the retinal nerve fibre layer in progressive multiple sclerosis using optical coherence tomography. Brain 131:277–287PubMed
6.
go back to reference Naismith RT, Tutlam NT, Xu J, Klawiter EC, Shepherd J, Trinkaus K, Song SK, Cross AH (2009) Optical coherence tomography differs in neuromyelitis optica compared with multiple sclerosis. Neurology 72:1077–1082CrossRefPubMed Naismith RT, Tutlam NT, Xu J, Klawiter EC, Shepherd J, Trinkaus K, Song SK, Cross AH (2009) Optical coherence tomography differs in neuromyelitis optica compared with multiple sclerosis. Neurology 72:1077–1082CrossRefPubMed
7.
go back to reference Ratchford JN, Quigg ME, Conger A, Frohman T, Frohman E, Balcer LJ, Calabresi PA, Kerr DA (2009) Optical coherence tomography helps differentiate neuromyelitis optica and MS optic neuropathies. Neurology 73:302–308CrossRefPubMed Ratchford JN, Quigg ME, Conger A, Frohman T, Frohman E, Balcer LJ, Calabresi PA, Kerr DA (2009) Optical coherence tomography helps differentiate neuromyelitis optica and MS optic neuropathies. Neurology 73:302–308CrossRefPubMed
8.
go back to reference 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 (2011) Primary retinal pathology in multiple sclerosis as detected by optical coherence tomography. Brain 134:518–533CrossRefPubMed 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 (2011) Primary retinal pathology in multiple sclerosis as detected by optical coherence tomography. Brain 134:518–533CrossRefPubMed
9.
go back to reference Saidha S, Syc SB, Durbin MK, Eckstein C, Oakley JD, Meyer SA, Conger A, Frohman TC, Newsome S, Ratchford JN, Frohman EM, Calabresi PA (2011) Visual dysfunction in multiple sclerosis correlates better with optical coherence tomography derived estimates of macular ganglion cell layer thickness than peripapillary retinal nerve fiber layer thickness. Multiple Scler 17:1449–1463CrossRef Saidha S, Syc SB, Durbin MK, Eckstein C, Oakley JD, Meyer SA, Conger A, Frohman TC, Newsome S, Ratchford JN, Frohman EM, Calabresi PA (2011) Visual dysfunction in multiple sclerosis correlates better with optical coherence tomography derived estimates of macular ganglion cell layer thickness than peripapillary retinal nerve fiber layer thickness. Multiple Scler 17:1449–1463CrossRef
10.
go back to reference Luo X, Frishman LJ (2011) Retinal pathway origins of the pattern electroretinogram (PERG). Invest Ophthalmol Vis Sci 52:8571–8584CrossRefPubMed Luo X, Frishman LJ (2011) Retinal pathway origins of the pattern electroretinogram (PERG). Invest Ophthalmol Vis Sci 52:8571–8584CrossRefPubMed
11.
go back to reference Hood DC, Xu L, Thienprasiddhi P, Greenstein VC, Odel JG, Grippo TM, Liebmann JM, Ritch R (2005) The pattern electroretinogram in glaucoma patients with confirmed visual field deficits. Invest Ophthalmol Vis Sci 46:2411–2418CrossRefPubMed Hood DC, Xu L, Thienprasiddhi P, Greenstein VC, Odel JG, Grippo TM, Liebmann JM, Ritch R (2005) The pattern electroretinogram in glaucoma patients with confirmed visual field deficits. Invest Ophthalmol Vis Sci 46:2411–2418CrossRefPubMed
12.
go back to reference Holder GE (2001) Pattern electroretinography (PERG) and an integrated approach to visual pathway diagnosis. Prog Retin Eye Res 20:531–561CrossRefPubMed Holder GE (2001) Pattern electroretinography (PERG) and an integrated approach to visual pathway diagnosis. Prog Retin Eye Res 20:531–561CrossRefPubMed
13.
go back to reference Celesia GG, Kaufman D, Cone SB (1986) Simultaneous recording of pattern electroretinography and visual evoked potentials in multiple sclerosis. A method to separate demyelination from axonal damage to the optic nerve. Arch Neurol 43:1247–1252CrossRefPubMed Celesia GG, Kaufman D, Cone SB (1986) Simultaneous recording of pattern electroretinography and visual evoked potentials in multiple sclerosis. A method to separate demyelination from axonal damage to the optic nerve. Arch Neurol 43:1247–1252CrossRefPubMed
14.
go back to reference Holder GE (1991) The incidence of abnormal pattern electroretinography in optic nerve demyelination. Electroencephalogr Clin Neurophysiol 78:18–26CrossRefPubMed Holder GE (1991) The incidence of abnormal pattern electroretinography in optic nerve demyelination. Electroencephalogr Clin Neurophysiol 78:18–26CrossRefPubMed
15.
go back to reference Holder GE (1997) The pattern electroretinogram in anterior visual pathway dysfunction and its relationship to the pattern visual evoked potential: a personal clinical review of 743 eyes. Eye 11(Pt 6):924–934CrossRefPubMed Holder GE (1997) The pattern electroretinogram in anterior visual pathway dysfunction and its relationship to the pattern visual evoked potential: a personal clinical review of 743 eyes. Eye 11(Pt 6):924–934CrossRefPubMed
16.
go back to reference Parisi V, Manni G, Spadaro M, Colacino G, Restuccia R, Marchi S, Bucci MG, Pierelli F (1999) Correlation between morphological and functional retinal impairment in multiple sclerosis patients. Invest Ophthalmol Vis Sci 40:2520–2527PubMed Parisi V, Manni G, Spadaro M, Colacino G, Restuccia R, Marchi S, Bucci MG, Pierelli F (1999) Correlation between morphological and functional retinal impairment in multiple sclerosis patients. Invest Ophthalmol Vis Sci 40:2520–2527PubMed
17.
go back to reference Almarcegui C, Dolz I, Pueyo V, Garcia E, Fernandez FJ, Martin J, Ara JR, Honrubia F (2010) Correlation between functional and structural assessments of the optic nerve and retina in multiple sclerosis patients. Neurophysiol Clin/Clin Neurophysiol 40:129–135CrossRef Almarcegui C, Dolz I, Pueyo V, Garcia E, Fernandez FJ, Martin J, Ara JR, Honrubia F (2010) Correlation between functional and structural assessments of the optic nerve and retina in multiple sclerosis patients. Neurophysiol Clin/Clin Neurophysiol 40:129–135CrossRef
18.
go back to reference Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, Fujihara K, Havrdova E, Hutchinson M, Kappos L, Lublin FD, Montalban X, O’Connor P, Sandberg-Wollheim M, Thompson AJ, Waubant E, Weinshenker B, Wolinsky JS (2011) Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol 69:292–302CrossRefPubMed Polman CH, Reingold SC, Banwell B, Clanet M, Cohen JA, Filippi M, Fujihara K, Havrdova E, Hutchinson M, Kappos L, Lublin FD, Montalban X, O’Connor P, Sandberg-Wollheim M, Thompson AJ, Waubant E, Weinshenker B, Wolinsky JS (2011) Diagnostic criteria for multiple sclerosis: 2010 revisions to the McDonald criteria. Ann Neurol 69:292–302CrossRefPubMed
19.
go back to reference Wingerchuk DM, Lennon VA, Pittock SJ, Lucchinetti CF, Weinshenker BG (2006) Revised diagnostic criteria for neuromyelitis optica. Neurology 66:1485–1489CrossRefPubMed Wingerchuk DM, Lennon VA, Pittock SJ, Lucchinetti CF, Weinshenker BG (2006) Revised diagnostic criteria for neuromyelitis optica. Neurology 66:1485–1489CrossRefPubMed
20.
go back to reference Scott TF (2007) Nosology of idiopathic transverse myelitis syndromes. Acta Neurol Scand 115:371–376CrossRefPubMed Scott TF (2007) Nosology of idiopathic transverse myelitis syndromes. Acta Neurol Scand 115:371–376CrossRefPubMed
21.
go back to reference Costello F, Coupland S, Hodge W, Lorello GR, Koroluk J, Pan YI, Freedman MS, Zackon DH, Kardon RH (2006) Quantifying axonal loss after optic neuritis with optical coherence tomography. Ann Neurol 59:963–969CrossRefPubMed Costello F, Coupland S, Hodge W, Lorello GR, Koroluk J, Pan YI, Freedman MS, Zackon DH, Kardon RH (2006) Quantifying axonal loss after optic neuritis with optical coherence tomography. Ann Neurol 59:963–969CrossRefPubMed
22.
go back to reference Holder GE, Brigell MG, Hawlina M, Meigen T, Vaegan, Bach M, International Society for Clinical Electrophysiology of V (2007) ISCEV standard for clinical pattern electroretinography–2007 update. Doc Ophthalmol Adv Ophthalmol 114:111–116 Holder GE, Brigell MG, Hawlina M, Meigen T, Vaegan, Bach M, International Society for Clinical Electrophysiology of V (2007) ISCEV standard for clinical pattern electroretinography–2007 update. Doc Ophthalmol Adv Ophthalmol 114:111–116
23.
go back to reference Garway-Heath DF, Poinoosawmy D, Fitzke FW, Hitchings RA (2000) Mapping the visual field to the optic disc in normal tension glaucoma eyes. Ophthalmology 107:1809–1815CrossRefPubMed Garway-Heath DF, Poinoosawmy D, Fitzke FW, Hitchings RA (2000) Mapping the visual field to the optic disc in normal tension glaucoma eyes. Ophthalmology 107:1809–1815CrossRefPubMed
24.
go back to reference Wang M, Hood DC, Cho JS, Ghadiali Q, De Moraes CG, Zhang X, Ritch R, Liebmann JM (2009) Measurement of local retinal ganglion cell layer thickness in patients with glaucoma using frequency-domain optical coherence tomography. Arch Ophthalmol 127:875–881CrossRefPubMed Wang M, Hood DC, Cho JS, Ghadiali Q, De Moraes CG, Zhang X, Ritch R, Liebmann JM (2009) Measurement of local retinal ganglion cell layer thickness in patients with glaucoma using frequency-domain optical coherence tomography. Arch Ophthalmol 127:875–881CrossRefPubMed
25.
go back to reference Hood DC, Cho J, Raza AS, Dale EA, Wang M (2011) Reliability of a computer-aided manual procedure for segmenting optical coherence tomography scans. Optom Vis Sci 88:113–123CrossRefPubMed Hood DC, Cho J, Raza AS, Dale EA, Wang M (2011) Reliability of a computer-aided manual procedure for segmenting optical coherence tomography scans. Optom Vis Sci 88:113–123CrossRefPubMed
26.
go back to reference DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837–845CrossRefPubMed DeLong ER, DeLong DM, Clarke-Pearson DL (1988) Comparing the areas under two or more correlated receiver operating characteristic curves: a nonparametric approach. Biometrics 44:837–845CrossRefPubMed
27.
go back to reference Parisi V (2003) Correlation between morphological and functional retinal impairment in patients affected by ocular hypertension, glaucoma, demyelinating optic neuritis and Alzheimer’s disease. Semin Ophthal 18:50–57 Parisi V (2003) Correlation between morphological and functional retinal impairment in patients affected by ocular hypertension, glaucoma, demyelinating optic neuritis and Alzheimer’s disease. Semin Ophthal 18:50–57
28.
go back to reference Ventura LM, Porciatti V, Ishida K, Feuer WJ, Parrish RK 2nd (2005) Pattern electroretinogram abnormality and glaucoma. Ophthalmology 112:10–19CrossRefPubMed Ventura LM, Porciatti V, Ishida K, Feuer WJ, Parrish RK 2nd (2005) Pattern electroretinogram abnormality and glaucoma. Ophthalmology 112:10–19CrossRefPubMed
29.
go back to reference Cunha LP, Oyamada MK, Monteiro ML (2008) Pattern electroretinograms for the detection of neural loss in patients with permanent temporal visual field defect from chiasmal compression. Doc Ophthalmol 117:223–232CrossRefPubMed Cunha LP, Oyamada MK, Monteiro ML (2008) Pattern electroretinograms for the detection of neural loss in patients with permanent temporal visual field defect from chiasmal compression. Doc Ophthalmol 117:223–232CrossRefPubMed
30.
go back to reference Monteiro ML, Cunha LP, Costa-Cunha LV, Maia OO Jr, Oyamada MK (2009) Relationship between optical coherence tomography, pattern electroretinogram and automated perimetry in eyes with temporal hemianopia from chiasmal compression. Invest Ophthalmol Vis Sci 50:3535–3541CrossRefPubMed Monteiro ML, Cunha LP, Costa-Cunha LV, Maia OO Jr, Oyamada MK (2009) Relationship between optical coherence tomography, pattern electroretinogram and automated perimetry in eyes with temporal hemianopia from chiasmal compression. Invest Ophthalmol Vis Sci 50:3535–3541CrossRefPubMed
31.
go back to reference Berninger TA, Heider W (1990) Pattern electroretinograms in optic neuritis during the acute stage and after remission. Graefes Arch Clin Exp Ophthalmol 228:410–414CrossRefPubMed Berninger TA, Heider W (1990) Pattern electroretinograms in optic neuritis during the acute stage and after remission. Graefes Arch Clin Exp Ophthalmol 228:410–414CrossRefPubMed
32.
go back to reference Falsini B, Porciatti V (1996) The temporal frequency response function of pattern ERG and VEP: changes in optic neuritis. Electroencephalogr Clin Neurophysiol 100:428–435PubMed Falsini B, Porciatti V (1996) The temporal frequency response function of pattern ERG and VEP: changes in optic neuritis. Electroencephalogr Clin Neurophysiol 100:428–435PubMed
33.
go back to reference Stefano E, Cupini LM, Rizzo P, Pierelli F, Rizzo PA (1991) Simultaneous recording of pattern electroretinogram (PERG) and visual evoked potential (VEP) in multiple sclerosis. Acta Neurol Belg 91:20–28PubMed Stefano E, Cupini LM, Rizzo P, Pierelli F, Rizzo PA (1991) Simultaneous recording of pattern electroretinogram (PERG) and visual evoked potential (VEP) in multiple sclerosis. Acta Neurol Belg 91:20–28PubMed
34.
go back to reference Graham SL, Wong VA, Drance SM, Mikelberg FS (1994) Pattern electroretinograms from hemifields in normal subjects and patients with glaucoma. Invest Ophthalmol Vis Sci 35:3347–3356PubMed Graham SL, Wong VA, Drance SM, Mikelberg FS (1994) Pattern electroretinograms from hemifields in normal subjects and patients with glaucoma. Invest Ophthalmol Vis Sci 35:3347–3356PubMed
35.
go back to reference Falsini B, Porrello G, Porciatti V, Fadda A, Salgarello T, Piccardi M (1999) The spatial tuning of steady state pattern electroretinogram in multiple sclerosis. Eur J Neurol 6:151–162CrossRefPubMed Falsini B, Porrello G, Porciatti V, Fadda A, Salgarello T, Piccardi M (1999) The spatial tuning of steady state pattern electroretinogram in multiple sclerosis. Eur J Neurol 6:151–162CrossRefPubMed
36.
37.
go back to reference Raza AS, Cho J, de Moraes CG, Wang M, Zhang X, Kardon RH, Liebmann JM, Ritch R, Hood DC (2011) Retinal ganglion cell layer thickness and local visual field sensitivity in glaucoma. Arch Ophthalmol 129:1529–1536CrossRefPubMed Raza AS, Cho J, de Moraes CG, Wang M, Zhang X, Kardon RH, Liebmann JM, Ritch R, Hood DC (2011) Retinal ganglion cell layer thickness and local visual field sensitivity in glaucoma. Arch Ophthalmol 129:1529–1536CrossRefPubMed
38.
go back to reference Monteiro ML, Hokazono K, Cunha LP, Oyamada MK (2012) Multifocal pattern electroretinography for the detection of neural loss in eyes with permanent temporal hemianopia or quadrantanopia from chiasmal compression. Br J Ophthalmol 96:104–109CrossRefPubMed Monteiro ML, Hokazono K, Cunha LP, Oyamada MK (2012) Multifocal pattern electroretinography for the detection of neural loss in eyes with permanent temporal hemianopia or quadrantanopia from chiasmal compression. Br J Ophthalmol 96:104–109CrossRefPubMed
Metadata
Title
Pattern electroretinogram in neuromyelitis optica and multiple sclerosis with or without optic neuritis and its correlation with FD-OCT and perimetry
Authors
Kenzo Hokazono
Ali S. Raza
Maria K. Oyamada
Donald C. Hood
Mário L. R. Monteiro
Publication date
01-12-2013
Publisher
Springer Berlin Heidelberg
Published in
Documenta Ophthalmologica / Issue 3/2013
Print ISSN: 0012-4486
Electronic ISSN: 1573-2622
DOI
https://doi.org/10.1007/s10633-013-9401-2

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