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Multifocal electroretinogram in diabetic macular edema and its correlation with different optical coherence tomography features

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Abstract

Purpose

To evaluate multifocal electroretinogram (mfERG) parameters in eyes with diabetic macular edema (DME) and its correlation with vision and optical coherence tomography (OCT) features.

Methods

Fifty-four eyes of 27 subjects with DME due to nonproliferative diabetic retinopathy were evaluated. MfERG responses were measured in three concentric rings. Macular thickness was measured by OCT in each segment of the three concentric rings, and mfERG rings were superimposed on the macular thickness map. The correlation between macular thickness in specific points of the thickness map and changes of the mfERG parameters in the corresponding points of the mfERG field map was evaluated and the relationship between the OCT and mfERG changes and changes of best-corrected visual acuity (BCVA) was investigated. The central foveal B-scans of SD-OCT were used to evaluate any correlation between the external limiting membrane (ELM) status, ellipsoid zone (EZ) status, presence of cysts or disorganization of retinal inner layers (DRIL), and mfERG parameters at the central corresponding area.

Results

The mean of BCVA was 0.5 ± 0.3 in logMAR, and the central macular thickness was 392.6 ± 123.4 microns. The central ring P1 and N2 amplitudes had a significant correlation with BCVA in univariate and multivariate analyses (P = 0.001 for both, r = − 0.346 and r = − 0.646, respectively). There was a significant correlation between retinal thickness and the N1 amplitude in the central ring (P = 0.02, r = − 0.343). Outer retinal layer disruption (ELM and EZ) correlated with prolonged P1 implicit time at the corresponding location (P = 0.005, r = 0.068). The presence of the DRIL was associated with reduced P1 and N2 amplitudes (P = 0.037, r = − 0.284 and P = 0.019, r = − 0.562, respectively). A significant correlation was also found between the presence of cysts and a lower central P1 amplitude (P = 0.033, r = − 0.376).

Conclusion

In diabetic patients, discrete changes of some parameters in the central ring of the mfERG field map (e.g., P1 and N2 amplitudes) have a significant correlation with both structural OCT abnormalities in the corresponding points of the thickness map (like DRIL, intraretinal cyst and ELM/EZ disruption) and BCVA. Predictive models such as those described in this report may make it possible to identify the relationship between specific anatomical and functional characteristics in diabetic retinopathy.

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References

  1. Williams R, Airey M, Baxter H, Forrester J, Kennedy-Martin T, Girach A (2004) Epidemiology of diabetic retinopathy and macular oedema: a systematic review. Eye (London, England) 18:963–983. https://doi.org/10.1038/sj.eye.6701476

    Article  CAS  Google Scholar 

  2. Hendrick AM, Gibson MV, Kulshreshtha A (2015) Diabetic retinopathy. Prim Care 42:451–464. https://doi.org/10.1016/j.pop.2015.05.005

    Article  PubMed  Google Scholar 

  3. Nagesh BN, Takkar B, Azad S, Azad R (2016) Optical coherence tomography and multifocal electroretinography in diabetic macular edema: a neurovascular relation with vision. Ophthalmic Surg Lasers Imaging Retina 47:626–631. https://doi.org/10.3928/23258160-20160707-03

    Article  CAS  PubMed  Google Scholar 

  4. Petropoulos IN, Green P, Chan AW, Alam U, Fadavi H, Marshall A, Asghar O, Efron N, Tavakoli M, Malik RA (2015) Corneal confocal microscopy detects neuropathy in patients with type 1 diabetes without retinopathy or microalbuminuria. PLoS ONE 10:e0123517. https://doi.org/10.1371/journal.pone.0123517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Adams AJ, Bearse MA Jr (2012) Retinal neuropathy precedes vasculopathy in diabetes: a function-based opportunity for early treatment intervention? Clin Exp Optom 95:256–265. https://doi.org/10.1111/j.1444-0938.2012.00733.x

    Article  PubMed  Google Scholar 

  6. Tehrani NM, Riazi-Esfahani H, Jafarzadehpur E, Mirzajani A, Talebi H, Amini A, Mazloumi M, Roohipoor R, Riazi-Esfahani M (2015) Multifocal electroretinogram in diabetic macular edema; correlation with visual acuity and optical coherence tomography. J Ophthalmic Vis Res 10:165–171. https://doi.org/10.4103/2008-322x.163773

    Article  PubMed  PubMed Central  Google Scholar 

  7. Hood DC (2000) Assessing retinal function with the multifocal technique. Prog Retin Eye Res 19:607–646

    Article  CAS  Google Scholar 

  8. Hood DC, Bach M, Brigell M, Keating D, Kondo M, Lyons JS, Marmor MF, McCulloch DL, Palmowski-Wolfe AM (2012) ISCEV standard for clinical multifocal electroretinography (mfERG) (2011 edition). Doc Ophthalmol Adv Ophthalmol 124:1–13. https://doi.org/10.1007/s10633-011-9296-8

    Article  Google Scholar 

  9. Zhu Y, Zhang T, Wang KY, Xu GZ (2014) Prognostic value of multifocal electroretinography and optical coherence tomography in eyes undergoing panretinal photocoagulation for diabetic retinopathy. Investig Ophthalmol Vis Sci 55:6358–6364. https://doi.org/10.1167/iovs.14-14704

    Article  Google Scholar 

  10. Harrison WW, Bearse MA Jr, Ng JS, Jewell NP, Barez S, Burger D, Schneck ME, Adams AJ (2011) Multifocal electroretinograms predict onset of diabetic retinopathy in adult patients with diabetes. Investig Ophthalmol Vis Sci 52:772–777. https://doi.org/10.1167/iovs.10-5931

    Article  Google Scholar 

  11. Yip YW, Ngai JW, Fok AC, Lai RY, Li H, Lam DS, Lai TY (2010) Correlation between functional and anatomical assessments by multifocal electroretinography and optical coherence tomography in central serous chorioretinopathy. Doc Ophthalmol Adv Ophthalmol 120:193–200. https://doi.org/10.1007/s10633-010-9213-6

    Article  Google Scholar 

  12. Serizawa S, Ohkoshi K, Minowa Y, Soejima K (2016) Interdigitation zone band restoration after treatment of diabetic macular edema. Curr Eye Res 41:1229–1234. https://doi.org/10.3109/02713683.2015.1113430

    Article  CAS  PubMed  Google Scholar 

  13. Das R, Spence G, Hogg RE, Stevenson M, Chakravarthy U (2018) Disorganization of inner retina and outer retinal morphology in diabetic macular edema. JAMA Ophthalmol 136:202–208. https://doi.org/10.1001/jamaophthalmol.2017.6256

    Article  PubMed  PubMed Central  Google Scholar 

  14. Azad R, Ghatak U, Sharma YR, Chandra P (2012) Multifocal electroretinogram in normal emmetropic subjects: correlation with optical coherence tomography. Indian J Ophthalmol 60:49–52. https://doi.org/10.4103/0301-4738.91345

    Article  PubMed  PubMed Central  Google Scholar 

  15. Ou WC, Brown DM, Payne JF, Wykoff CC (2017) Relationship between visual acuity and retinal thickness during anti-vascular endothelial growth factor therapy for retinal diseases. Am J Ophthalmol 180:8–17. https://doi.org/10.1016/j.ajo.2017.05.014

    Article  CAS  PubMed  Google Scholar 

  16. Diabetic Retinopathy Clinical Research N, Browning DJ, Glassman AR, Aiello LP, Beck RW, Brown DM, Fong DS, Bressler NM, Danis RP, Kinyoun JL, Nguyen QD, Bhavsar AR, Gottlieb J, Pieramici DJ, Rauser ME, Apte RS, Lim JI, Miskala PH (2007) Relationship between optical coherence tomography-measured central retinal thickness and visual acuity in diabetic macular edema. Ophthalmology 114:525–536. https://doi.org/10.1016/j.ophtha.2006.06.052

    Article  Google Scholar 

  17. Holm K, Larsson J, Lovestam-Adrian M (2007) In diabetic retinopathy, foveal thickness of 300 mum seems to correlate with functionally significant loss of vision. Doc Ophthalmol Adv Ophthalmol 114:117–124. https://doi.org/10.1007/s10633-006-9044-7

    Article  Google Scholar 

  18. Dale EA, Hood DC, Greenstein VC, Odel JG (2010) A comparison of multifocal ERG and frequency domain OCT changes in patients with abnormalities of the retina. Doc Ophthalmol Adv Ophthalmol 120:175–186. https://doi.org/10.1007/s10633-009-9210-9

    Article  Google Scholar 

  19. Goel N, Prakash A, Gupta AK (2018) Multifocal electroretinography in diabetic retinopathy with and without macular edema. Ophthalmic Surg Lasers Imaging Retina 49:780–786. https://doi.org/10.3928/23258160-20181002-06

    Article  PubMed  Google Scholar 

  20. Murakami T, Nishijima K, Sakamoto A, Ota M, Horii T, Yoshimura N (2011) Association of pathomorphology, photoreceptor status, and retinal thickness with visual acuity in diabetic retinopathy. Am J Ophthalmol 151:310–317. https://doi.org/10.1016/j.ajo.2010.08.022

    Article  PubMed  Google Scholar 

  21. Yamamoto S, Yamamoto T, Hayashi M, Takeuchi S (2001) Morphological and functional analyses of diabetic macular edema by optical coherence tomography and multifocal electroretinograms. Graefe’s Arch Clin Exp Ophthalmol 239:96–101

    Article  CAS  Google Scholar 

  22. Sun JK, Lin MM, Lammer J, Prager S, Sarangi R, Silva PS, Aiello LP (2014) Disorganization of the retinal inner layers as a predictor of visual acuity in eyes with center-involved diabetic macular edema. JAMA Ophthalmol 132:1309–1316. https://doi.org/10.1001/jamaophthalmol.2014.2350

    Article  PubMed  Google Scholar 

  23. Sun JK, Radwan SH, Soliman AZ, Lammer J, Lin MM, Prager SG, Silva PS, Aiello LB, Aiello LP (2015) Neural retinal disorganization as a robust marker of visual acuity in current and resolved diabetic macular edema. Diabetes 64:2560–2570. https://doi.org/10.2337/db14-0782

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Radwan SH, Soliman AZ, Tokarev J, Zhang L, van Kuijk FJ, Koozekanani DD (2015) Association of disorganization of retinal inner layers with vision after resolution of center-involved diabetic macular edema. JAMA Ophthalmol 133:820–825. https://doi.org/10.1001/jamaophthalmol.2015.0972

    Article  PubMed  Google Scholar 

  25. Pelosini L, Hull CC, Boyce JF, McHugh D, Stanford MR, Marshall J (2011) Optical coherence tomography may be used to predict visual acuity in patients with macular edema. Investig Ophthalmol Vis Sci 52:2741–2748. https://doi.org/10.1167/iovs.09-4493

    Article  Google Scholar 

  26. Deak GG, Bolz M, Ritter M, Prager S, Benesch T, Schmidt-Erfurth U, Diabetic Retinopathy Research Group V (2010) A systematic correlation between morphology and functional alterations in diabetic macular edema. Investig Ophthalmol Vis Sci 51:6710–6714. https://doi.org/10.1167/iovs.09-5064

    Article  Google Scholar 

  27. Alkuraya H, Kangave D, Abu El-Asrar AM (2005) The correlation between optical coherence tomographic features and severity of retinopathy, macular thickness and visual acuity in diabetic macular edema. Int Ophthalmol 26:93–99. https://doi.org/10.1007/s10792-006-9007-8

    Article  PubMed  Google Scholar 

  28. Klemp K, Larsen M, Sander B, Vaag A, Brockhoff PB, Lund-Andersen H (2004) Effect of short-term hyperglycemia on multifocal electroretinogram in diabetic patients without retinopathy. Investig Ophthalmol Vis Sci 45:3812–3819. https://doi.org/10.1167/iovs.03-1260

    Article  Google Scholar 

  29. Saxena S, Ruia S, Prasad S, Jain A, Mishra N, Natu SM, Meyer CH, Gilhotra JS, Kruzliak P, Akduman L (2017) Increased serum levels of urea and creatinine are surrogate markers for disruption of retinal photoreceptor external limiting membrane and inner segment ellipsoid zone in type 2 diabetes mellitus. Retina 37:344–349. https://doi.org/10.1097/IAE.0000000000001163

    Article  CAS  PubMed  Google Scholar 

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Correspondence to Hamid Riazi-Esfahani.

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Khojasteh, H., Riazi-Esfahani, H., Khalili Pour, E. et al. Multifocal electroretinogram in diabetic macular edema and its correlation with different optical coherence tomography features. Int Ophthalmol 40, 571–581 (2020). https://doi.org/10.1007/s10792-019-01215-4

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