Optical Coherence Tomography and Multifocal Electroretinography in Diabetic Macular Edema: A Neurovascular Relation With Vision
Abstract
BACKGROUND AND OBJECTIVES:
To evaluate retinal neuropathy in patients with diabetic macular edema (DME) with multifocal electroretinograph (mfERG), and to evaluate the simultaneous impact of retinal neuropathy and vasculopathy on visual acuity in subtypes of DME.
PATIENTS AND METHODS:
This prospective, controlled, investigative study conducted at a tertiary eye care center of Northern India included 79 eyes of 50 treatment-naïve patients with DME (Group 1), 94 eyes of 50 diabetic patients without diabetic retinopathy (Group 2), and 100 eyes of 100 normal volunteers as controls. Comprehensive ocular evaluation along with mfERG and optical coherence tomography (OCT) were performed for all patients. N1 and P1 mfERG waveforms in the two central-most rings of macula were evaluated for amplitudes and implicit time. OCT was used to sub-classify types of DME and evaluate macular thickness, ellipsoid zone (EZ), and external limiting membrane (ELM) disruption. Best-corrected visual acuity (BCVA) relative to other variables was the primary outcome measure. The three groups were compared for all the parameters inclusive of OCT and mfERG patterns. Further, OCT subtypes of DME were analyzed for mfERG waveform patterns.
RESULTS:
All mfERG values were significantly lower in Group 1 and Group 2 as compared to Group 3 (P < .05). BCVA strongly correlated with central macular thickness, EZ, and ELM disruption scores in Group 1 (P = .001), but correlated modestly with mfERG waveform amplitudes in Group 1 patients with intact EZ and ELM only. BCVA correlated with mfERG amplitudes in patients with neurosensory detachment, but not in those with cystoid macular edema.
CONCLUSIONS:
Neural changes set in before the clinical changes related to vasculopathy manifest in diabetic patients. Neuroretinopathy in patients with DME affects all retinal layers symmetrically in early stages, but impacts the middle retinal layers severely in advanced disease form. BCVA correlates with electrophysiological changes till the time morphological features are visible when stronger correlation is seen with anatomical disruption.
[Ophthalmic Surg Lasers Imaging Retina. 2016;47:626–631.]
- 1.Foos RY. Chronic retinopathy of prematurity. Ophthalmology. 1985; 92(4):563–574.
10.1016/S0161-6420(85)34007-1 Crossref Medline, Google Scholar - 2.Tehrani NM, Riazi-Esfahani H, Jafarzadehpur E, Multifocal electroretinogram in diabetic macular edema; correlation with visual acuity and optical coherence tomography. J Ophthalmic Vis Res. 2015; 10(2):165–171.
10.4103/2008-322X.163773 Crossref Medline, Google Scholar - 3.No authors listed. Treatment techniques and clinical guidelines for photocoagulation of diabetic macular edema. Early Treatment Diabetic Retinopathy Study Report Number 2. Ophthalmology. 1987; 94(7):761–774.
10.1016/S0161-6420(87)33527-4 Crossref Medline, Google Scholar - 4.Petropoulos IN, Green P, Chan AWS, Corneal confocal microscopy detects neuropathy in patients with Type 1 diabetes without retinopathy or microalbuminuria. PLoS ONE. 2015; 10(4):e0123517.
10.1371/journal.pone.0123517 Crossref Medline, Google Scholar - 5.Adams AJ, Bearse MA. Retinal neuropathy precedes vasculopathy in diabetes: a function-based opportunity for early treatment intervention?Clin Exp Optom. 2012; 95(3):256–265.
10.1111/j.1444-0938.2012.00733.x Crossref Medline, Google Scholar - 6.Hood DC, Bach M, Brigell M, ISCEV standard for clinical multifocal electroretinography (mfERG) (2011 edition). Doc Ophthalmol. 2012; 124(1):1–13.
10.1007/s10633-011-9296-8 Crossref Medline, Google Scholar - 7.Staurenghi G, Sadda S, Chakravarthy U, Proposed lexicon for anatomic landmarks in normal posterior segment spectral-domain optical coherence tomography: the IN•OCT consensus. Ophthalmology. 2014; 121(8):1572–1578.
10.1016/j.ophtha.2014.02.023 Crossref Medline, Google Scholar - 8.Panozzo G, Parolini B, Gusson E, Diabetic macular edema: an OCT-based classification. Semin Ophthalmol. 2004; 19(1–2):13–20.
10.1080/08820530490519934 Crossref Medline, Google Scholar - 9.Panozzo G, Gusson E, Parolini B, Role of OCT in the diagnosis and follow up of diabetic macular edema. Semin Ophthalmol. 2003; 18(2):74–81.
10.1076/soph.18.2.74.15854 Crossref Medline, Google Scholar - 10.Maheshwary AS, Oster SF, Yuson RM, Cheng L, Mojana F, Freeman WR. The association between percent disruption of the photoreceptor inner segment-outer segment junction and visual acuity in diabetic macular edema. Am J Ophthalmol. 2010; 150(1):63–67.e1.
10.1016/j.ajo.2010.01.039 Crossref Medline, Google Scholar - 11.Shimada Y, Li Y, Bearse MA, Sutter EE, Fung W. Assessment of early retinal changes in diabetes using a new multifocal ERG protocol. Br J Ophthalmol. 2001; 85(4):414–419.
10.1136/bjo.85.4.414 Crossref Medline, Google Scholar - 12.Fortune B, Schneck ME, Adams AJ. Multifocal electroretinogram delays reveal local retinal dysfunction in early diabetic retinopathy. Invest Ophthalmol Vis Sci. 1999; 40(11):2638–2651. Medline, Google Scholar
- 13.Han Y, Bearse MA, Schneck ME, Barez S, Jacobsen CH, Adams AJ. Multifocal electroretinogram delays predict sites of subsequent diabetic retinopathy. Invest Ophthalmol Vis Sci. 2004; 45(3):948–954.
10.1167/iovs.03-1101 Crossref Medline, Google Scholar - 14.Ng JS, Bearse MA, Schneck ME, Barez S, Adams AJ. Local diabetic retinopathy prediction by multifocal ERG delays over 3 years. Invest Ophthalmol Vis Sci. 2008; 49(4):1622–1628.
10.1167/iovs.07-1157 Crossref Medline, Google Scholar - 15.Kang H1, Xu YS, Zhang H, Du B. Characters of multifocal electroretinogram in different grades of diabetic macular edema. Zhonghua Yan Ke Za Zhi. 2011; 47(8):709–714. Medline, Google Scholar
- 16.Bearse MA, Ozawa GY. Multifocal electroretinography in diabetic retinopathy and diabetic macular edema. Curr Diab Rep. 2014; 14(9):526.
10.1007/s11892-014-0526-9 Crossref Medline, Google Scholar - 17.Schneck ME, Bearse MA, Han Y, Barez S, Jacobsen C, Adams AJ. Comparison of mfERG waveform components and implicit time measurement techniques for detecting functional change in early diabetic eye disease. Doc Ophthalmol. 2004; 108(3):223–230.
10.1007/s10633-004-8745-z Crossref Medline, Google Scholar - 18.Greenstein VC, Holopigian K, Hood DC, Seiple W, Carr RE. The nature and extent of retinal dysfunction associated with diabetic macular edema. Invest Ophthalmol Vis Sci. 2000; 41(11):3643–3654. Medline, Google Scholar
- 19.Venkatesh P, Ramanjulu R, Azad R, Vohra R, Garg S. Subthreshold micropulse diode laser and double frequency neodymium: YAG laser in treatment of diabetic macular edema: a prospective, randomized study using multifocal electroretinography. Photomed Laser Surg. 2011; 29(11):727–733.
10.1089/pho.2010.2830 Crossref Medline, Google Scholar - 20.Kim YM, Lee SY, Koh HJ. Prediction of postoperative visual outcome after pars plana vitrectomy based on preoperative multifocal electroretinography in eyes with diabetic macular edema. Graefes Arch Clin Exp Ophthalmol. 2010; 248(10):1387–1393.
10.1007/s00417-010-1398-6 Crossref Medline, Google Scholar - 21.Durukan AH, Memisoglu S, Gundogan FC. Is multifocal ERG a reliable index of macular function after triamcinolone acetonide injection in diffuse diabetic macular edema?Eur J Ophthalmol. 2009; 19(6):1017–1027. Crossref Medline, Google Scholar
- 22.Wu D, Jiang F, Liang J, Multifocal electroretinogram in cystoid macular edema. Yan Ke Xue Bao. 2003; 19(4):253–256. Medline, Google Scholar
- 23.Lung JC, Swann PG, Wong DS, Chan HH. Global flash multifocal electroretinogram: early detection of local functional changes and its correlations with optical coherence tomography and visual field tests in diabetic eyes. Doc Ophthalmol. 2012; 125(2):123–135.
10.1007/s10633-012-9343-0 Crossref Medline, Google Scholar - 24.Dale EA, Hood DC, Greenstein VC, Odel JG. A comparison of multifocal ERG and frequency domain OCT changes in patients with abnormalities of the retina. Doc Ophthalmol. 2010; 120(2):175–186.
10.1007/s10633-009-9210-9 Crossref Medline, Google Scholar - 25.Yamamoto S, Yamamoto T, Hayashi M, Takeuchi S. Morphological and functional analyses of diabetic macular edema by optical coherence tomography and multifocal electroretinograms. Graefes Arch Clin Exp Ophthalmol. 2001; 239(2):96–101.
10.1007/s004170000238 Crossref Medline, Google Scholar - 26.Tripathy K, Sharma YR, Karthikeya R, Recent advances in management of diabetic macular edema. Curr Diabetes Rev. 2015; 11(2):79–97.
10.2174/1573399811999150324120640 Crossref Medline, Google Scholar

