Exogenous Factors Affecting Multifocal Electroretinogram: A mini review

Authors

  • Ai-Hong Chen Optometry & Visual Sciences Research Centre (iROViS), Faculty of Health Sciences, Universiti Teknologi MARA (UiTM) Puncak Alam Campus, 42300 Puncak Alam, Selangor, Malaysia. http://orcid.org/0000-0003-4568-0495
  • Muhamad Syukri Mohamad Rafiuddin Universiti Teknologi MARA https://orcid.org/0000-0002-8159-5071
  • Stuart Coupland University of Ottawa

DOI:

https://doi.org/10.5384/sjovs.v14i1.123

Keywords:

multifocal electroretinogram, exogenous factors, mfERG measurements, clinical interpretation

Abstract

Multifocal electroretinogram (mfERG) is an important diagnostic tool in the clinical evaluation of central electro-retinal function of the macula. To enhance the diagnostic values and to improve its accuracy and internal consistency, it is crucial to examine carefully the endogenous and exogenous factors that affect mfERG recordings and clinical interpretations. This mini review focuses on three aspects of exogenous factors including (1) physiological variations pertaining to age and gender; (2) systemic changes owing to oxygen, blood pressure and glucose levels; (3) individual variables due to refractive status, pupil size,  luminance and viewing condition.

References

Alavi, M. V. (2016). Aging and vision. Advances in experimental medicine and biology (pp. 393–399). Springer New York LLC. https://doi.org/10.1007/978- 3- 319- 17121- 0_52

Albrecht, J., Jägle, H., Hood, D. C., & Sharpe, L. T. (2002). The multifocal electroretinogram (mfERG) and cone isolating stimuli: Variation in L- and M-cone driven signals across the retina. Journal of Vision, 2(8), 543–558. https://doi. org/10.1167/2.8.2

Bearse, M. A., & Sutter, E. E. (1996). Imaging localized retinal dysfunction with the multifocal electroretinogram. Journal of the Optical Society of America A, 13(3), 634–640. https://doi.org/10.1364/JOSAA.13.000634

Bellmann, C., Neveu, M. M., Kousoulides, L., Sloper, J. J., Bird, A. C., & Holder, G. E. (2004). Potential diagnostic dilemmas using the multifocal electroretinogram in intermittent exotropia [1]. British Journal of Ophthalmology, 88(9), 1223–1224. https://doi.org/10.1136/bjo.2003.040584

Bonnel, S., Mohand-Said, S., & Sahel, J. A. (2003). The aging of the retina. Experimental Gerontology, 38(8), 825–831. https://doi.org/10.1016/S0531-5565(03) 00093-7

Boynton, R. M. (1953). Stray light and the human electroretinogram. Journal of the Optical Society of America, 43(6), 442–449. https://doi.org/10.1364/JOSA.43. 000442

Chan, H. L., & Brown, B. (2000). Pilot study of the multifocal electroretinogram in ocular hypertension. British Journal of Ophthalmology, 84(10), 1147–1153. https://doi.org/10.1136/bjo.84.10.1147

Chan, H. L., & Mohidin, N. (2003). Variation of multifocal electroretinogram with axial length. Ophthalmic and Physiological Optics, 23(2), 133–140. https://doi.org/10.1046/j.1475-1313.2003.00097.x

Chappelow, A. V., & Marmor, M. F. (2002). Effects of pre-adaptation conditions and ambient room lighting on the multifocal ERG. Documenta Ophthalmologica, 105(1), 23–31. https://doi.org/10.1023/A:1015713029443

Chen, J. C., Brown, B., & Schmid, K. L. (2006a). Changes in implicit time of the multifocal electroretinogram response following contrast adaptation. Current Eye Research, 31(6), 549–556. https://doi.org/10.1080/02713680600744869

Chen, J. C., Brown, B., & Schmid, K. L. (2006b). Delayed mfERG responses in myopia. Vision Research, 46(8-9), 1221–1229. https://doi.org/10.1016/j.visres.2005.06.030

Chisholm, J. A., Keating, D., Parks, S., & Evans, A. L. (2001). The impact of fixation on the multifocal electroretinogram. Documenta Ophthalmologica, 102(2), 131–139. https://doi.org/10.1023/A:1017536625847

Chu, P. H. W., Chan, H. L., & Leat, S. J. (2006). Effects of unsteady fixation on multifocal electroretinogram (mfERG). Graefe’s Archive for Clinical and Experimental Ophthalmology, 244(10), 1273–1282. https://doi.org/10.1007/s00417-006-0304-8

Creel, D. J. (2019). Electroretinograms. Handbook of clinical neurology (pp. 481– 493). Elsevier B.V. https://doi.org/10.1016/B978-0-444-64032-1.00032-1

Feigl, B., Stewart, I., & Brown, B. (2007). Experimental hypoxia in human eyes: Implications for ischaemic disease. Clinical Neurophysiology, 118(4), 887–895. https://doi.org/10.1016/j.clinph.2006.12.012

Fortune, B., & Johnson, C. A. (2002). Decline of photopic multifocal electroretinogram responses with age is due primarily to preretinal optical factors. Journal of the Optical Society of America A: Optics and Image Science, and Vision, 19(1), 173–184. https://doi.org/10.1364/JOSAA.19.000173

Gerth, C., Garcia, S. M., Ma, L., Keltner, J. L., & Werner, J. S. (2002). Multifocal electroretinogram: Age-related changes for different luminance levels. Graefe’s Archive for Clinical and Experimental Ophthalmology, 240(3), 202–208. https://doi.org/10.1007/s00417-002-0442-6

Gonzalez, P., Parks, S., Dolan, F., & Keating, D. (2004). The effects of pupil size on the multifocal electroretinogram. Documenta Ophthalmologica, 109(1), 67–72. https://doi.org/10.1007/s10633-004-1545-7

Gundogan, F. C., Isilak, Z., Erdurman, C., Mumcuoglu, T., Durukan, A. H., & Bayraktar, M. Z. (2008). Multifocal electroretinogram in mild to moderate essential hypertension. Clinical and Experimental Hypertension, 30(5), 375–384. https: //doi.org/10.1080/10641960802275148

Harrison, W. W., Benson, A., Fetkin, S., Havens, A., Lyon, E., & Yevseyenkov, V. (2014). Multifocal electroretinogram amplitudes are associated with mean ocular perfusion pressure in patients with diabetes and vascular disease. Investigative Ophthalmology & Visual Science, 55 (13), 338–338.

Heinemann-Vernaleken, B., Palmowski, A., & Allgayer, R. (2000). The effect of time of day and repeat reliability on the fast flicker multifocal ERG. Documenta Ophthalmologica, 101(3), 247–255. https://doi.org/10.1023/A:1002898112128

Hood, D. C. (2000). Assessing retinal function with the multifocal technique. Progress in Retinal and Eye Research, 19(5), 607–646. https://doi.org/10.1016/ S1350- 9462(00)00013-6

Hood, D. C., Bach, M., Brigell, M., Keating, D., Kondo, M., Lyons, J. S., Marmor, M. F., McCulloch, D. L., & Palmowski-Wolfe, A. M. (2012). ISCEV standard for clinical multifocal electroretinography (mfERG) (2011 edition). Documenta Ophthalmologica, 124(1), 1–13. https://doi.org/10.1007/s10633-011-9296-8

Hood, D. C., Bach, M., Brigell, M., Keating, D., Kondo, M., Lyons, J. S., & Palmowski-Wolfe, A. M. (2008). ISCEV guidelines for clinical multifocal electroretinography (2007 edition). Documenta Ophthalmologica, 116(1), 1–11. https://doi.org/10.1007/s10633-007-9089-2

Hood, D. C., Odel, J. G., Chen, C. S., & Winn, B. J. (2003). The multifocal electroretinogram. Journal of Neuro-Ophthalmology, 23(3), 225–235. https://doi.org/ 10.1097/00041327- 200309000- 00008

Jackson, G. R., Ortega, J. D. L., Girkin, C., Rosenstiel, C. E., & Owsley, C. (2002). Aging-related changes in the multifocal electroretinogram. Journal of the Optical Society of America A: Optics and Image Science, and Vision, 19(1), 185–189. https://doi.org/10.1364/JOSAA.19.000185

Jägle, H., Heine, J., & Kurtenbach, A. (2006). L:M-cone ratio estimates of the outer and inner retina and its impact on sex differences in ERG amplitudes. Documenta Ophthalmologica, 113(2), 105–113. https://doi.org/10.1007/s10633-006-9019-8

Kaltwasser, C., Horn, F. K., Kremers, J., & Juenemann, A. (2009). A comparison of the suitability of cathode ray tube (CRT) and liquid crystal display (LCD) monitors as visual stimulators in mfERG diagnostics. Documenta Ophthalmologica, 118(3), 179–189. https://doi.org/10.1007/s10633-008-9152-7

Keating, D., Parks, S., & Evans, A. (2000). Technical aspects of multifocal ERG recording. Documenta Ophthalmologica, 100 (2-3), 77–98. https://doi.org/10.1023/ a:1002723501303

Khan, M. I., Barlow, R. B., & Weinstock, R. S. (2011). Acute hypoglycemia decreases central retinal function in the human eye. Vision Research, 51(14), 1623–1626. https://doi.org/10.1016/j.visres.2011.05.003

Kim, C. B. Y., Ver Hoeve, J. N., Kaufman, P. L., & Nork, T. M. (2004). Interspecies and gender differences in multifocal electroretinograms of cynomolgus and rhesus macaques. Documenta Ophthalmologica, 109(1), 73–86. https://doi.org/10.1007/ s10633- 004- 2630- 7

Kim, J. W., Choi, Y. J., Lee, S. Y., & Choi, K. S. (2013). Clinical usefulness of binocular multifocal electroretinography in patients with monocular macular disease. Korean journal of Ophthalmology : KJO, 27 (4), 261–267. https://doi.org/10. 3341/kjo.2013.27.4.261

Klemp, K., Lund-Andersen, H., Sander, B., & Larsen, M. (2007). The effect of acute hypoxia and hyperoxia on the slow multifocal electroretinogram in healthy subjects. Investigative Ophthalmology and Visual Science, 48(7), 3405–3412. https: //doi.org/10.1167/iovs.06-0471

Klemp, K., Sander, B., Brockhoff, P. B., Vaag, A., Lund-Andersen, H., & Larsen, M. (2005). The multifocal ERG in diabetic patients without retinopathy during euglycemic clamping. Investigative Ophthalmology and Visual Science, 46(7), 2620– 2626. https://doi.org/10.1167/iovs.04-1254

Kofoed, P. K., Sander, B., Zubieta-Calleja, G., Kessel, L., Klemp, K., & Larsen, M. (2009). The effect of high– to low–altitude adaptation on the multifocal electroretinogram. Investigative Ophthalmology and Visual Science, 50(8), 3964– 3969. https://doi.org/10.1167/iovs.08-3216

Kondo, M., Miyake, Y., Piao, C. H., Tanikawa, A., Horiguchi, M., & Terasaki, H. (1999). Amplitude increase of the multifocal electroretinogram during light adaptation. Investigative Ophthalmology and Visual Science, 40(11), 2633–2637. https://www.scopus.com/inward/record.uri?eid=2-s2.0-0032830643&partnerID=40& md5=1364f423e3b48977224fde03c9e08bc4

Lu, X. J., Zhang, F. W., Cheng, L., Liu, A. Q., & Duan, J. G. (2011). Effect on mul- tifocal electroretinogram in persistently elevated intraocular pressure by erigeron breviscapus extract. International Journal of Ophthalmology, 4(4), 349–352. https://doi.org/10.3980/j.issn.2222-3959.2011.04.04

Luu, C. D., Lau, A. M. I., & Lee, S. Y. (2006). Multifocal electroretinogram in adults and children with myopia. Archives of Ophthalmology, 124(3), 328–334. https://doi.org/10.1001/archopht.124.3.328

Man, R. E. K., Lamoureux, E. L., Taouk, Y., Xie, J., Sasongko, M. B., Best, W. J., Noonan, J. E., Kawasaki, R., Wang, J. J., & Luu, C. D. (2013). Axial length, retinal function, and oxygen consumption: A potential mechanism for a lower risk of dia- betic retinopathy in longer eyes. Investigative Ophthalmology and Visual Science, 54(12), 7691–7698. https://doi.org/10.1167/iovs.13-12412

Marmor, M. F., Hood, D. C., Keating, D., Kondo, M., Seeliger, M. W., & Miyake, Y. (2003). Guidelines for basic multifocal electroretinography (mfERG). Documenta Ophthalmologica, 106(2), 105–115. https://doi.org/10.1023/A:1022591317907

Michael Nork, T., Kim, C. B. Y., Heatley, G. A., Kaufman, P. L., Lucarelli, M. J., Levin, L. A., & Ver Hoeve, J. N. (2010). Serial multifocal electroretinograms during long-term elevation and reduction of intraocular pressure in non-human primates. Documenta Ophthalmologica, 120(3), 273–289. https://doi.org/10.1007/s10633- 010- 9231- 4

Mohamad-Rafiuddin, M.-S., Rosli, S. A., Chen, A.-H., & Wan-Hamat, W.-N. (2014). The effects of non-dilated and dilated pupil at different eccentricity on multifocal electroretinogram. Investigative Ophthalmology & Visual Science, 55(13), 348– 348.

Mokdad, A. H., Ford, E. S., Bowman, B. A., Dietz, W. H., Vinicor, F., Bales, V. S., & Marks, J. S. (2003). Prevalence of obesity, diabetes, and obesity-related health risk factors, 2001. Journal of the American Medical Association, 289(1), 76–79. https://doi.org/10.1001/jama.289.1.76

Nabeshima, T., Tazawa, Y., Mita, M., & Sano, M. (2002). Effects of aging on the first and second-order kernels of multifocal electroretinogram. Japanese Journal of Ophthalmology, 46 (3), 261–269. https://doi.org/10.1016/S0021- 5155(02)00475- 6

Ozawa, G. Y., Bearse, M. A., Harrison, W. W., Bronson-Castain, K. W., Schneck, M. E., Barez, S., & Adams, A. J. (2014). Differences in neuroretinal function between adult males and females. Optometry and Vision Science, 91(6), 602–607.

https://doi.org/10.1097/OPX.0000000000000255

Pálffy, A., Janáky, M., Fejes, I., Horváth, G., & Benedek, G. (2010). Interocular amplitude differences of multifocal electroretinograms obtained under monocular and binocular stimulation conditions. Acta Physiologica Hungarica, 97(3), 326– 331. https://doi.org/10.1556/APhysiol.97.2010.3.9

Palmowski, A. M., Berninger, T., Allgayer, R., Andrielis, H., Heinemann-Vernaleken, B., & Rudolph, G. (1999). Effects of refractive blur on the multifocal electroretinogram. Documenta Ophthalmologica, 99(1), 41–54. https://doi.org/10. 1023/A:1002432113628

Panorgias, A., Tillman, M., Sutter, E. E., Moshiri, A., Gerth-Kahlert, C., & Werner, J. S. (2017). Senescent changes and topography of the dark-adapted multifocal electroretinogram. Investigative Ophthalmology and Visual Science, 58(2), 1323– 1329. https://doi.org/10.1167/iovs.16-20953

Pappachan, J. M., Chacko, E. C., Arunagirinathan, G., & Sriraman, R. (2011). Man- agement of hypertension and diabetes in obesity: Non-pharmacological measures. International Journal of Hypertension, 2011. https://doi.org/10.4061/2011/398065

Pavlidis, M., Stupp, T., Georgalas, I., Georgiadou, E., Moschos, M., & Thanos, S. (2005). Multifocal electroretinography changes in the macula at high altitude: A report of three cases. Ophthalmologica, 219(6), 404–412. https://doi.org/10.1159/ 000088387

Poloschek, C. M., & Bach, M. (2009a). Can we do without mydriasis in multifocal ERG recordings? Documenta Ophthalmologica, 118(2), 121–127. https://doi.org/ 10.1007/s10633- 008- 9146- 5

Poloschek, C. M., & Bach, M. (2009b). The mfERG response topography with scaled stimuli: Effect of the stretch factor. Documenta Ophthalmologica, 119(51), 51–58. https://doi.org/10.1007/s10633- 009- 9169- 6

Read, S. A., Collins, M. J., & Iskander, D. R. (2008). Diurnal variation of axial length, intraocular pressure, and anterior eye biometrics. Investigative Ophthalmology and Visual Science, 49(7), 2911–2918. https://doi.org/10.1167/iovs.08- 1833

Robson, A. G., Nilsson, J., Li, S., Jalali, S., Fulton, A. B., Tormene, A. P., Holder, G. E., & Brodie, S. E. (2018). ISCEV guide to visual electrodiagnostic procedures. Documenta Ophthalmologica, 136 (1). https://doi.org/10.1007/s10633- 017- 9621- y

Rosli, S. A., Chen, A.-H., Che Alwi, N.-F., & Mohamad-Rafiuddin, M.-S. (2014). The effect of induced meridional refractive defocus on the amplitude and implicit time of multifocal electroretinogram (mfERG). Investigative Ophthalmology & Visual Science, 55 (13), 3501–3501.

Rudolph, G., Kalpadakis, P., Jurklies, B., & Sutter, E. (2002). The role of fixation for reliable mfERG results (multiple letters) [3]. Graefe’s Archive for Clinical and Experimental Ophthalmology, 240 (10), 874–875. https://doi.org/10.1007/s00417- 002- 0549- 9

Sachidanandam, R., Ravi, P., & Sen, P. (2017). Effect of axial length on full-field and multifocal electroretinograms. Clinical and Experimental Optometry, 100(6), 668–675. https://doi.org/10.1111/cxo.12529

Sandberg, M. A., Berson, E. L., & Ariel, M. (1977). Visually evoked response testing with a stimulator-ophthalmoscope: Macular scars, hereditary macular degenerations, and retinitis pigmentosa. Archives of Ophthalmology, 95(10), 1805–1808. https://doi.org/10.1001/archopht.1977.04450100107013

Sandberg, M. A., Hanson, A. H., & Berson, E. L. (1983). Foveal and parafoveal cone electroretinograms in juvenile macular degeneration. Ophthalmic Genetics, 3 (2), 83–87. https://doi.org/10.3109/13816818309007823

Saul, A. B., & Still, A. E. (2017). Multifocal electroretinography in the presence of temporal and spatial correlations and eye movements. Vision (Switzerland), 1(1). https://doi.org/10.3390/vision1010003

Schimitzek, T., & Bach, M. (2006). The influence of luminance on the multifocal ERG. Documenta Ophthalmologica, 113 (3), 187–192. https://doi.org/10.1007/s10633- 006- 9028- 7

Seiple, W., Szlyk, J. P., Paliga, J., & Rabb, M. F. (2006). Perifoveal function in patients with North Carolina macular dystrophy: The importance of accounting for fixation locus. Investigative Ophthalmology and Visual Science, 47 (4), 1703–1709. https://doi.org/10.1167/iovs.05-0659

Shimada, Y., & Horiguchi, M. (2003). Stray light-induced multifocal electroretinograms. Investigative Ophthalmology and Visual Science, 44(3), 1245–1251. https://doi.org/10.1167/iovs.02-0527

Suresh, S., Tienor, B. J., Smith, S. D., & Lee, M. S. (2016). The effects of fun- dus photography on the multifocal electroretinogram. Documenta Ophthalmolog- ica, 132 (1), 39–45. https://doi.org/10.1007/s10633- 016- 9525- 2

Sutter, E. E., & Tran, D. (1992). The field topography of ERG components in man-I. the photopic luminance response. Vision Research, 32 (3), 433–446. https://doi.org/10.1016/0042-6989(92)90235- B

Tsang, S. H., & Sharma, T. (2018). Electroretinography. Advances in experimental medicine and biology (pp. 17–20). Springer New York LLC. https://doi.org/10. 1007/978- 3- 319- 95046- 4_5

Turnbull, P. R. K., Goodman, L. K., & Phillips, J. R. (2020). Global-flash mfERG responses to local differences in spherical and astigmatic defocus across the human retina. Ophthalmic and Physiological Optics, 40(1), 24–34. https://doi.org/10. 1111/opo.12656

Tzekov, R. T., Gerth, C., & Werner, J. S. (2004). Senescence of human multifocal electroretinogram components: A localized approach. Graefe’s Archive for Clini- cal and Experimental Ophthalmology, 242(7), 549–560. https://doi.org/10.1007/ s00417- 004- 0892- 0

Vogelmeier, C. F., Criner, G. J., Martinez, F. J., Anzueto, A., Barnes, P. J., Bourbeau, J., Celli, B. R., Chen, R., Decramer, M., Fabbri, L. M., Frith, P., Halpin, D. M. G., López Varela, M. V., Nishimura, M., Roche, N., Rodriguez-Roisin, R., Sin, D. D., Singh, D., Stockley, R., ... Agusti, A. (2017). Global strategy for the diagnosis, management and prevention of chronic obstructive lung disease 2017 report: GOLD executive summary. Respirology, 22(3), 575–601. https://doi.org/ 10.1111/resp.13012

Vrabec, T. R., Affel, E. L., Gaughan, J. P., Foroozan, R., Tennant, M. T. S., Klancnik Jr, J. M., Jordan, C. S., & Savino, P. J. (2004). Voluntary suppression of the multifocal electroretinogram. Ophthalmology, 111(1), 169–176. https://doi.org/10.1016/j.ophtha.2003.04.011

Wirth, A., & Zetterstrom, B. (1954). Effect of area and intensity on the size and shape of the electroretinogram; exclusion of stray light effects. The British Journal of Ophthalmology, 38(5), 257–265. https://doi.org/10.1136/bjo.38.5.257

Wolsley, C. J., Saunders, K. J., Silvestri, G., & Anderson, R. S. (2008). Investiga- tion of changes in the myopic retina using multifocal electroretinograms, optical coherence tomography and peripheral resolution acuity. Vision Research, 48(14), 1554–1561. https://doi.org/10.1016/j.visres.2008.04.013

Ziccardi, L., Lombardo, G., Parisi, V., Serrao, S., & Lombardo, M. (2014). Parafoveal cone metrics and their relationship with multifocal electroretinogram. Investigative Ophthalmology & Visual Science, 55(13), 2620–2620.

Downloads

Published

2021-07-14

How to Cite

Chen, A.-H., Mohamad Rafiuddin , M. S. ., & Coupland, S. (2021). Exogenous Factors Affecting Multifocal Electroretinogram: A mini review. Scandinavian Journal of Optometry and Visual Science, 14(1), 1–9. https://doi.org/10.5384/sjovs.v14i1.123

Issue

Section

Review Article