Skip to main content

Advertisement

SpringerLink
Log in

A meta-analysis of clinical electro-oculography values

  • Original Research Article
  • Published:
Documenta Ophthalmologica Aims and scope Submit manuscript

Abstract

Background

The aim of the meta-analysis was to derive a range of mean normal clinical electrooculogram (EOG) values from a systematic review of published EOG studies that followed the guidelines of the ISCEV standard for clinical electro-oculography.

Methods

A systematic literature review was performed using four relevant databases limited to peer-reviewed articles in English between 1967 and February 2017. Studies reporting clinical EOG or FO normal values were included when the report used a standard 30° horizontal saccade, a retinal luminance of between 100 and 250 cd m−2, and had > 10 subjects in their normative values. The search identified 1145 articles after duplicates were removed with subsequent screening of the abstracts excluding a further 1098, resulting in 47 full-text articles that were then assessed by the author (PC) with a final nine articles meeting the inclusion criteria. An overall effect estimate using inverse variance-weighted meta-analysis was performed to estimate the mean values for the light peak/dark trough ratio (LP:DT ratio) (dilated and undilated), the time to the LP, the amplitude of the LP, dark trough (DT) and the fast oscillation (FO) peak-to-trough ratio from the included studies.

Results

The mean dilated LP:DT ratio was 2.35 (95% CI 2.28–2.42); undilated LP:DT ratio was 2.37 (95% CI 2.28–2.45); LP amplitude was 835 (95% CI 631–1039) µV and the mean time to the LP being 8.2 (95% CI 7.7–8.7) min. The mean DT amplitude was 358 (95% CI 292–424) µV, and the mean FO peak-to-trough ratio was 1.13 (95% CI 1.11–1.16). The results of the LP/DT ratio are drawn from studies with a mean ± standard deviation (SD) age of 34.08 ± 12.93 years for dilated and 33.65 ± 12.28 years for undilated LP/DT ratios.

Conclusions

The meta-analysis of EOG studies has generated a reference range of normal mean values for clinicians to refer to when using the ISCEV clinical EOG. It provides a potential method to generate similar data sets from published normal values in related visual electrophysiology tests.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Constable PA, Bach M, Frishman LJ, Jeffrey BG, Robson AG (2017) ISCEV Standard for clinical electro-oculography (2017 update). Doc Ophthalmol 134(1):1–9

    Article  PubMed  PubMed Central  Google Scholar 

  2. McCulloch DL, Marmor MF, Brigell MG, Hamilton R, Holder GE, Tzekov R et al (2015) 2015) ISCEV Standard for full-field clinical electroretinography (2015 update. Doc Ophthal 130(1):1–12

    Article  Google Scholar 

  3. Odom JV, Bach M, Brigell M, Holder GE, McCulloch DL, Mizota A et al (2016) ISCEV standard for clinical visual evoked potentials: (2016 update). Doc Ophthalmol 133(1):1–9

    Article  PubMed  Google Scholar 

  4. Hood DC, Bach M, Brigell M, Keating D, Kondo M, Lyons JS, et al (2012) ISCEV standard for clinical multifocal electroretinography (mfERG) (2011 edition). Doc Ophthalmol 124(1):1-13

  5. Brigell M, Bach M, Barber C, Moskowitz A, Robson J (2003) Guidelines for calibration of stimulus and recording parameters used in clinical electrophysiology of vision. Doc Ophthal 107(2):185–193

    Article  Google Scholar 

  6. Marmor MF, Zrenner E (1993) Standard for clinical electro-oculography. International Society for Clinical Electrophysiology of Vision. Doc Ophthalmol 85(2):115–124

    Article  CAS  PubMed  Google Scholar 

  7. Marmor MF (1998) Standardization notice: EOG standard reapproved. Electro-oculogram. Doc Ophthalmol. 95(1):91–92

    Article  CAS  PubMed  Google Scholar 

  8. Brown M, Marmor M, Vaegan Zrenner E, Brigell M, Bach M (2006) ISCEV Standard for Clinical Electro-oculography (EOG). Doc Ophthalmol 113(3):205–212

    Article  PubMed  PubMed Central  Google Scholar 

  9. Marmor MF, Brigell MG, McCulloch DL, Westall CA, Bach M (2011) ISCEV standard for clinical electro-oculography (2010 update). Doc Ophthalmol 122(1):1–7

    Article  PubMed  Google Scholar 

  10. Arden GB, Barrada A, Kelsey JH (1962) A new clinical test of retinal function based upon the standing potential of the eye. Brit J Ophthalmol 46:449–467

    Article  CAS  Google Scholar 

  11. Arden GB, Constable PA (2006) The electro-oculogram. Progress in Retinal & Eye Research 25(2):207–248

    Article  Google Scholar 

  12. Constable PA (2014) A perspective on the mechanism of the light-rise of the electrooculogram. IOVS 55(4):2669–2673

    CAS  Google Scholar 

  13. Demet EM, Albers L, Sokolski KN, Chicz-Demet A, Chen CC, Reist C (1997) Apomorphine induced alteration in corneofundal potentials in depression. Prog Neuro-Psychopharmacology & Biological Psychiatry 21(5):775–788

    Article  CAS  Google Scholar 

  14. Inoue M, Tamai A, Hatta S, Sasaki Y (2003) Slow and Fast Oscillation Electrooculography in Central Retinal Vein Occlusion: a Comparison between Affected Eyes and Fellow Intact Eyes. Yonago Acta Med 46(3):65–75

    Google Scholar 

  15. Nakao H, Miki N, Nagata M, Sasaki Y, Yamasaki A, Endo M et al (1995) Fast oscillations of the electro-oculogram in a series of normal subjects. Jap J Ophthalmol 39(2):113–119

    CAS  Google Scholar 

  16. Ozaki N, Rosenthal NE, Moul DE, Schwartz PJ, Oren DA (1993) Effects of phototherapy Winter seasonal affective-disorder on electrooculographic ratio in Winter seasonal affective-disorder. Psychiat Res 49(2):99–107

    Article  CAS  Google Scholar 

  17. Türksever C, Orgül S, Todorova MG (2015) Comparing short-duration electro-oculograms with and without mydriasis in healthy subjects. Klin Monatsbl Augenheilkd 232(4):471–476

    Article  PubMed  Google Scholar 

  18. Schneck ME, Fortune B, Adams AJ (2000) The fast oscillation of the electrooculogram reveals sensitivity of the human outer retina/retinal pigment epithelium to glucose level. Vis Res 40(24):3447–3453

    Article  CAS  PubMed  Google Scholar 

  19. Zobor D, Strasser T, Zobor G, Schober F, Messias A, Strauss O et al (2015) Ophthalmological assessment of cannabis-induced persisting perception disorder: is there a direct retinal effect? Doc Ophthalmol 130(2):121–130

    Article  PubMed  Google Scholar 

  20. Moher D, Shamseer L, Clarke M, Ghersi D, Liberati A, Petticrew M et al (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Systematic Reviews 4(1):1

    Article  PubMed  PubMed Central  Google Scholar 

  21. Krogh E (1975) Normal values in clinical electrooculography: i. Material, method, methodological investigations and distribution of the potential and time parameters. Acta Ophthalmol 53(4):563–575

    Article  CAS  Google Scholar 

  22. Krogh E (1976) Normal values in clinical electrooculography: iI. Analysis of Potential and Time Parameters and Their Relation to Other Variables. Acta Ophthalmol 54(4):389–400

    Article  CAS  Google Scholar 

  23. Momirov D, van Lilh GHM, van der Torren K, Vijfvinkel-Bruinenga S (1982) Normal values of the basic level of the standing potential and its light rise. Ophthalmologica 184(4):225–231

    Article  CAS  PubMed  Google Scholar 

  24. Thaler A, Heilig P, Gordesch J (1976) Light peak to dark trough ratio in clinical electro-oculography: influence of dark oscillations on the following light peak. Bibliotheca ophthalmologica: supplementa ad ophthalmologica. 85:110–114

    Google Scholar 

  25. Ohn YH, Katsumi O, Kruger-Leite E, Larson EW, Hirose T (1991) Electrooculogram in central retinal vein obstruction. Ophthalmologica 203(4):189–195

    Article  CAS  PubMed  Google Scholar 

  26. Papakostopoulos D, Bloom PA, Grey RH, Dean Hart JC (1992) The electro-oculogram in central retinal vein occlusion. Brit J Ophthalmol 76(9):515–519

    Article  CAS  Google Scholar 

  27. Deng Y, Zhou H, Duan J (1994) Electro-oculogram of retinal vein occlusion. Yen Ko Hsueh Pao 10(1):60–64

    CAS  PubMed  Google Scholar 

  28. Hara A, Miura M (1994) Decreased inner retinal activity in branch retinal vein occlusion. Doc Ophthalmol 88(1):39–47

    Article  CAS  PubMed  Google Scholar 

  29. Hozo SP, Djulbegovic B, Hozo I (2005) Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 5(1):13

    Article  PubMed  PubMed Central  Google Scholar 

  30. Jackson SA (1979) The optimum illuminance level for clinical electro-oculography. Acta Ophthalmol 57(4):665–668

    Article  CAS  Google Scholar 

  31. Timmins N, Marmor MF (1992) Studies on the stability of the clinical electro-oculogram. Doc Ophthalmol 81(2):163–171

    Article  CAS  PubMed  Google Scholar 

  32. Lam RW, Beattie CW, Buchanan A, Remick RA, Zis AP (1991) Low electrooculographic ratios in patients with seasonal affective disorder. Amer J Psychiat 148(11):1526–1529

    Article  CAS  PubMed  Google Scholar 

  33. Seggie J, MacMillan H, Griffith L, Shannon HS, Martin J, Simpson J et al (1991) Retinal pigment epithelium response and the use of the EOG and arden ratio in depression. Psychiat Res 36(2):175–185

    Article  CAS  Google Scholar 

  34. Lubinski W, Zajaczek S, Sych Z, Penkala K, Palacz O, Lubinski J (2004) Supernormal electro-oculograms in patients with neurofibromatosis type 1. Hered 2(4):193–196

    Google Scholar 

  35. Marmor MF, Wu KH (2005) Alcohol- and light-induced electro-oculographic responses: variability and clinical utility. Doc Ophthalmol 110(2–3):227–236

    Article  PubMed  Google Scholar 

  36. Arden GB, Wolf JE (2000) The human electro-oculogram: interaction of light and alcohol. IOVS 41(9):2722–2729

    CAS  Google Scholar 

  37. Thavikulwat AT, Lopez P, Caruso RC, Jeffrey BG (2015) The effects of gender and age on the range of the normal human electro-oculogram. Doc Ophthalmol 131(3):177–188

    Article  PubMed  PubMed Central  Google Scholar 

  38. Caruso RC, Lopez P, Ayres LM, Kaiser-Kupfer MI (2003) Fast and slow oscillations of the electro-oculogram in Stargardt’s disease. IOVS 44:U712-U

  39. Thompson DA, Constable PA, Liasis A, Walters B, Esteban MT (2016) The physiology of the retinal pigment epithelium in Danon disease. Retina 36(3):629–638

    Article  CAS  PubMed  Google Scholar 

  40. Low S, Davidson AE, Holder GE, Hogg CR, Bhattacharya SS, Black GC et al (2011) Autosomal dominant Best disease with an unusual electrooculographic light rise and risk of angle-closure glaucoma: a clinical and molecular genetic study. Mol Vis 17:2272–2282

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Arden GB, Kelsey JH (1962) Some observations on the relationship between the standing potential of the human eye and bleaching and regeneration of visual purple. J Physiol (Lond) 161:205–226

    Article  CAS  Google Scholar 

  42. Ozaki N, Rosenthal NE, Myers F, Schwartz PJ, Oren DA (1995) Effects of season on electro-oculographic ratio in winter seasonal affective disorder. Psychiat Res 59(1–2):151–155

    Article  CAS  Google Scholar 

  43. Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327(7414):557–560

    Article  PubMed  PubMed Central  Google Scholar 

  44. Mergaerts F, Daems E, van Malderen L, Spileers W (2001) Recording of the fast oscillations in the human electro-oculogram. Doc Ophthalmol 103(1):63–72

    Article  CAS  PubMed  Google Scholar 

  45. Constable PA, Lawrenson JG, Arden GB (2006) Light and alcohol evoked electro-oculograms in cystic fibrosis. Doc Ophthalmol 113(3):133–143

    Article  PubMed  Google Scholar 

  46. De Rouck A, Kayembe D (1981) A clinical procedure for the simultaneous recording of fast and slow EOG oscillations. International Ophthalmol 3(3):179–189

    Article  Google Scholar 

  47. Thorburn W, Nordstrom S (1978) EOG in a large family with hereditary macular degeneration. (Best’s vitelliform macular dystrophy) identification of gene carriers. Acta Ophthalmol 56(3):455–464

    Article  CAS  Google Scholar 

  48. Schatz P, Bitner H, Sander B, Holfort S, Andreasson S, Larsen M et al (2010) Evaluation of macular structure and function by OCT and electrophysiology in patients with vitelliform macular dystrophy due to mutations in BEST1. IOVS 51(9):4754–4765

    Google Scholar 

  49. Weleber RG (1989) Fast and Slow oscillations of the electro-oculogram in Best’s Macular Dystrophy and Retinitis Pigmentosa. Arch Ophthalmol 107(4):530–537

    Article  CAS  PubMed  Google Scholar 

  50. Burgess R, Millar ID, Leroy BP, Urquhart JE, Fearon IM, De Baere E et al (2008) Biallelic mutation of BEST1 causes a distinct retinopathy in humans. Amer J Hum Genet 82(1):19–31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Xiao QH, Hartzell HC, Yu KA (2010) Bestrophins and retinopathies. Pflűgers Archiv-Eur J Physiol 460(2):559–569

    Article  CAS  Google Scholar 

  52. Boon CJF, van den Born LI, Visser L, Keunen JEE, Bergen AAB, Booij JC et al (2013) Autosomal Recessive Bestrophinopathy: differential diagnosis and treatment options. Ophthalmology 120(4):809–820

    Article  PubMed  Google Scholar 

  53. Crowley C, Paterson R, Lamey T, McLaren T, De Roach J, Chelva E et al (2014) Autosomal recessive bestrophinopathy associated with angle-closure glaucoma. Doc Ophthalmol 129(1):57–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Toto L, Boon CJ, Di Antonio L, Battaglia Parodi M, Mastropasqua R, Antonucci I et al (2016) Bestrophinopathy: a spectrum of ocular abnormalities caused by the c.614T > C mutation in the BEST1 Gene. Retina 36(8):1586–1595

    Article  CAS  PubMed  Google Scholar 

  55. Carter DA, Smart MJ, Letton WV, Ramsden CM, Nommiste B, Chen LL et al (2016) Mislocalisation of BEST1 in iPSC-derived retinal pigment epithelial cells from a family with autosomal dominant vitreoretinochoroidopathy (ADVIRC). Sci Rep 6:33792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Goldberg MF, Lee FL, Tso MO, Fishman GA (1989) Histopathologic study of autosomal dominant vitreoretinochoroidopathy. Peripheral annular pigmentary dystrophy of the retina. Ophthalmology 96(12):1736–1746

    Article  CAS  PubMed  Google Scholar 

  57. Yardley J, Leroy BP, Hart-Holden N, Lafaut BA, Loeys B, Messiaen LM et al (2004) Mutations of VMD2 splicing regulators cause nanophthalmos and autosomal dominant vitreoretinochoroidopathy (ADVIRC). IOVS 45(10):3683–3689

    Google Scholar 

  58. Derekoy S, Kenar F, Yavas GF, Kusbeci T, Ozturk F, Aycicek A (2016) The influence of iris color and retina pigment epithelium melanin on allergic rhinitis. Ent Updates. 6(1):23–28

    Article  Google Scholar 

  59. Lubinski W, Zajaczek S, Sych Z, Penkala K, Palacz O, Lubinski J (2001) Electro-oculogram in patients with neurofibromatosis type 1. Doc Ophthalmol 103(2):91–103

    Article  CAS  PubMed  Google Scholar 

  60. Williams C, Papakostopoulos D (1995) Electro-oculographic abnormalities in amblyopia. BJO 79(3):218–224

    CAS  Google Scholar 

  61. Pinckers A, Perret CM, Brink H (1990) The EOG in systemic disease: alopecia areata, lupus erythematodes, rheumatoid arthritis. Neuro-Ophthalmology 10(3):145–151

    Article  Google Scholar 

  62. Leguire LE, Pappa KS, McGregor ML, Rogers GL, Bremer DL (1992) Electro-oculogram in vitamin A deficiency associated with cystic fibrosis. Short communication. Ophthal Paediat Genet 13(3):187–189

    Article  CAS  PubMed  Google Scholar 

  63. Kimizuka Y, Kiyosawa M, Tamai M, Takase S (1993) Retinal changes in myotonic dystrophy: clinical and follow-up evaluation. Retina 13(2):129–135

    Article  CAS  PubMed  Google Scholar 

  64. O’Brien C, Duvall-Young J, Brown M, Short C, Bone M (1993) Electrophysiology of type II mesangiocapillary glomerulonephritis with associated fundus abnormalities. BJO 77(12):778–780

    Article  Google Scholar 

  65. Faktorovich EG, Kim RY (1996) Electrophysiologic and psychophysical abnormalities in a patient with membranoproliferative glomerulonephritis type II (dense-deposit disease) retinopathy. IOVS 37(3):S505

    Google Scholar 

  66. Ikeda H, Head GM, Ellis CJ (1994) Electrophysiological signs of retinal dopamine deficiency in recently diagnosed Parkinson’s disease and a follow up study. Vis Res 34(19):2629–2638

    Article  CAS  PubMed  Google Scholar 

  67. Reist C, Sokolski KN, Chen CC, Coskinas E, Demet EM (1995) The effect of sleep deprivation on motor impairment and retinal adaptation in Parkinson’s disease. Prog Neuro-Psychopharmacol Biol Psychiat 19(3):445–454

    Article  CAS  Google Scholar 

  68. Sokolski KN, Reist C, Chen CC, DeMet EM (1995) Antidepressant responses and changes in visual adaptation after sleep deprivation. Psychiat Res 57(3):197–207

    Article  CAS  Google Scholar 

  69. Rinaldi M, Libondi T, Cotticelli L, Rinaldi M, D’Onofrio C (1996) Electrofunctional study in Vitiligo patients without ocular changes. IOVS 37(3):S1037

    Google Scholar 

  70. Scuderi GL, Ricci F, Nucci C, Galasso MJ, Cerulli L (1998) Electro-oculography in pigment dispersion syndrome. Ophthalmic Res 30(1):23–29

    Article  CAS  PubMed  Google Scholar 

  71. Greenstein VC, Seiple W, Liebmann J, Ritch R (2001) Retinal pigment epithelial dysfunction in patients with pigment dispersion syndrome: implications for the theory of pathogenesis. Arch Ophthalmol 119(9):1291–1295

    Article  CAS  PubMed  Google Scholar 

  72. Arndt CF, Sari A, Ferre M, Parrat E, Courtas D, De Seze J et al (2001) Electrophysiological effects of corticosteroids on the retinal pigment epithelium. IOVS 42(2):472–475

    CAS  Google Scholar 

  73. Arden GB, Barrada A (1962) An analysis of the electrooculograms of a series of normal subjects. BJO 46:468–482

    Article  CAS  Google Scholar 

  74. Pinckers A (1979) Clinical electro-oculography. Acta Ophthalmol 57(4):623–632

    Article  CAS  Google Scholar 

  75. Adams A (1973) The normal electro-oculogram (E.O.G.). Acta Ophthalmol 51(4):551–561

    Article  CAS  Google Scholar 

  76. Krogh E (1977) Normal values in clinical electrooculography: III. Numerical evaluation of two dimensionless EOG Parameters. Acta Ophthalmol 55(2):227–236

    Article  CAS  Google Scholar 

  77. Thaler ARG, Lessel MR, Heilig P, Scheiber V (1982) The fast oscillation of the electro-oculogram. Influence of stimulus intensity and adaptation time on amplitude and peak latency. Ophthalmic Res 14(3):210–214

    Article  CAS  PubMed  Google Scholar 

  78. Trimble JL, Ernest JT, Newell FW (1977) Electro-oculography in infants. IOVS 16(7):668–670

    CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Ms. Nikki May from Flinders University Library services for help in conducting the literature search.

Author information

Authors and Affiliations

  1. College of Nursing and Health Sciences, Flinders University, GPO Box 2100, Adelaide, SA, 5001, Australia

    Paul A. Constable

  2. College of Medicine and Public Health, Flinders University, Adelaide, Australia

    David Ngo

  3. Department of Statistics, Data Science and Epidemiology, Swinburne University of Technology, Melbourne, Australia

    Stephen Quinn

  4. Clinical and Academic Department of Ophthalmology, Great Ormond Street Hospital for Children, London, UK

    Dorothy A. Thompson

  5. UCL Great Ormond Street Institute for Child Health, London, UK

    Dorothy A. Thompson

Authors
  1. Paul A. Constable
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. David Ngo
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Stephen Quinn
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dorothy A. Thompson
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Paul A. Constable.

Ethics declarations

Conflict of interest

All authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; educational grants; participation in speakers’ bureaus; membership, employment, consultancies, stock ownership, or other equity interest; and expert testimony or patent-licensing arrangements), or non-financial interest (such as personal or professional relationships, affiliations, knowledge or beliefs) in the subject matter or materials discussed in this manuscript.

Statement on the welfare of animals

This article does not contain any studies with animals performed by any of the authors.

Informed consent

For this type of study, formal consent is not required.

Statement of human rights

As this study does not contain any involvement of human or animal participants, ethical approval is not required or is applicable.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Constable, P.A., Ngo, D., Quinn, S. et al. A meta-analysis of clinical electro-oculography values. Doc Ophthalmol 135, 219–232 (2017). https://doi.org/10.1007/s10633-017-9616-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10633-017-9616-8

Keywords

Search

Navigation