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Published in: Documenta Ophthalmologica 2/2020

01-04-2020 | Diabetic Retinopathy | Original Research Article

Retinal vasculature–function correlation in non-proliferative diabetic retinopathy

Authors: Yunkao Zeng, Dan Cao, Dawei Yang, Xuenan Zhuang, Yunyan Hu, Miao He, Honghua Yu, Jun Wang, Cheng Yang, Liang Zhang

Published in: Documenta Ophthalmologica | Issue 2/2020

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Abstract

Purpose

To compare and correlate retinal microcirculation and function in patients with non-proliferative diabetic retinopathy (NPDR).

Methods

Thirty-three healthy controls (33 eyes), 36 diabetic patients with no clinically detectable retinopathy (NDR, 36 eyes) and 101 patients (101 eyes) with NPDR (35 mild NPDR, 34 moderate NPDR, 32 severe NPDR) were involved in the study. We used optical coherence tomography angiography (OCTA) to quantify the macular vessel density (VD) of superficial capillary plexus (SCP), deep capillary plexus (DCP) and foveal density in a 300 μm region around foveal avascular zone. Retinal function was assessed by a mydriasis-free, full-field flicker electroretinogram (FERG) recording device, and the amplitudes and implicit time were recorded. The association between microvascular parameters and FERG results was analyzed with stepwise multiple linear regression model.

Results

Decreased amplitudes and delayed implicit time, as well as lower parafoveal/perifoveal VD in both SCP and DCP, were found in NDR group and NPDR groups compared with the control group (all p < 0.05). Specifically, the FERG parameters and microvascular indices were comparable between NDR group and mild NPDR group (all p > 0.05). However, compared to mild NPDR, the reduction in FERG amplitude was more pronounced than the reduction in parafoveal VD (both SCP and DCP) in severe NPDR. Stepwise multiple linear regression analyses showed that delayed implicit time was significantly correlated with increased age and decreased VD of parafoveal region in both SCP and DCP in patients with NPDR. Meanwhile, decreased amplitude was significantly associated with decreased VD of parafoveal region in both SCP and DCP in patients with NPDR.

Conclusion

Macular VD in both superficial and deep capillary plexus correlated with ERG implicit time and amplitude in mild-to-severe NPDR. OCTA and FERG may both be useful in detection of preclinical DR and early DR, but once the disease deteriorates, FERG may be more sensitive to discern progression of DR.
Literature
1.
go back to reference Yau JWY, Rogers S, Kawasaki R, Lamoureux EL, Kowalski JW, Bek T, Chen S, Dekker JM, Fletcher AE, Grauslund J (2012) Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care 35(3):556–564CrossRef Yau JWY, Rogers S, Kawasaki R, Lamoureux EL, Kowalski JW, Bek T, Chen S, Dekker JM, Fletcher AE, Grauslund J (2012) Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care 35(3):556–564CrossRef
2.
go back to reference Ng JS, Bearse MA, Schneck ME, Barez S, Adams AJ (2008) Local diabetic retinopathy prediction by multifocal ERG delays over 3 years. Invest Ophthalmol Vis Sci 49(4):1622–1628CrossRef Ng JS, Bearse MA, Schneck ME, Barez S, Adams AJ (2008) Local diabetic retinopathy prediction by multifocal ERG delays over 3 years. Invest Ophthalmol Vis Sci 49(4):1622–1628CrossRef
3.
go back to reference Harrison WW, Bearse MA, 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. Invest Ophthalmol Vis Sci 52(2):772–777CrossRef Harrison WW, Bearse MA, 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. Invest Ophthalmol Vis Sci 52(2):772–777CrossRef
4.
go back to reference Bearse MA, Han Y, Schneck ME, Barez S, Jacobsen C, Adams AJ (2004) Local multifocal oscillatory potential abnormalities in diabetes and early diabetic retinopathy. Invest Ophthalmol Vis Sci 45(9):3259–3265CrossRef Bearse MA, Han Y, Schneck ME, Barez S, Jacobsen C, Adams AJ (2004) Local multifocal oscillatory potential abnormalities in diabetes and early diabetic retinopathy. Invest Ophthalmol Vis Sci 45(9):3259–3265CrossRef
6.
go back to reference Maa AY, Feuer WJ, Davis CQ, Pillow EK, Brown TD, Caywood RM, Chasan JE, Fransen SR (2016) A novel device for accurate and efficient testing for vision-threatening diabetic retinopathy. J Diabetes Complicat 30(3):524–532CrossRef Maa AY, Feuer WJ, Davis CQ, Pillow EK, Brown TD, Caywood RM, Chasan JE, Fransen SR (2016) A novel device for accurate and efficient testing for vision-threatening diabetic retinopathy. J Diabetes Complicat 30(3):524–532CrossRef
7.
go back to reference Fukuo M, Hirose A, Kitano S, Kato K, Kondo M (2016) Screening for diabetic retinopathy using RETevalTM, new mydriasis-free full-field ERG recording system. Invest Ophthalmol Vis Sci 57(12):6340 Fukuo M, Hirose A, Kitano S, Kato K, Kondo M (2016) Screening for diabetic retinopathy using RETevalTM, new mydriasis-free full-field ERG recording system. Invest Ophthalmol Vis Sci 57(12):6340
8.
go back to reference Bresnick GH, Palta M (1987) Temporal aspects of the electroretinogram in diabetic retinopathy. Arch Ophthalmol 105(5):660–664CrossRef Bresnick GH, Palta M (1987) Temporal aspects of the electroretinogram in diabetic retinopathy. Arch Ophthalmol 105(5):660–664CrossRef
9.
go back to reference Santos AR, Ribeiro L, Bandello F, Lattanzio R, Egan C, Frydkjaer-Olsen U, García-Arumí J, Gibson J, Grauslund J, Harding SP, Lang GE, Massin P, Midena E, Scanlon P, Aldington SJ, Simão S, Schwartz C, Ponsati B, Porta M, Costa MÂ, Hernández C, Cunha-Vaz J, Simó R (2017) Functional and structural findings of neurodegeneration in early stages of diabetic retinopathy: cross-sectional analyses of baseline data of the EUROCONDOR project. Diabetes 66(9):2503–2510. https://doi.org/10.2337/db16-1453 CrossRefPubMed Santos AR, Ribeiro L, Bandello F, Lattanzio R, Egan C, Frydkjaer-Olsen U, García-Arumí J, Gibson J, Grauslund J, Harding SP, Lang GE, Massin P, Midena E, Scanlon P, Aldington SJ, Simão S, Schwartz C, Ponsati B, Porta M, Costa MÂ, Hernández C, Cunha-Vaz J, Simó R (2017) Functional and structural findings of neurodegeneration in early stages of diabetic retinopathy: cross-sectional analyses of baseline data of the EUROCONDOR project. Diabetes 66(9):2503–2510. https://​doi.​org/​10.​2337/​db16-1453 CrossRefPubMed
10.
go back to reference Tyrberg M, Ponjavic V, Lovestamadrian M (2008) Multifocal electroretinogram (mfERG) in patients with diabetes mellitus and an enlarged foveal avascular zone (FAZ). Doc Ophthalmol 117(3):185–189CrossRef Tyrberg M, Ponjavic V, Lovestamadrian M (2008) Multifocal electroretinogram (mfERG) in patients with diabetes mellitus and an enlarged foveal avascular zone (FAZ). Doc Ophthalmol 117(3):185–189CrossRef
11.
go back to reference Jansson RW, Raeder MB, Krohn J (2015) Photopic full-field electroretinography and optical coherence tomography in type 1 diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol 253(7):989–997CrossRef Jansson RW, Raeder MB, Krohn J (2015) Photopic full-field electroretinography and optical coherence tomography in type 1 diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol 253(7):989–997CrossRef
12.
go back to reference Sandhu HS, Eladawi N, Elmogy M, Keynton RS, Helmy O, Schaal S, Elbaz A (2018) Automated diabetic retinopathy detection using optical coherence tomography angiography: a pilot study. Br J Ophthalmol 102(11):1564–1569CrossRef Sandhu HS, Eladawi N, Elmogy M, Keynton RS, Helmy O, Schaal S, Elbaz A (2018) Automated diabetic retinopathy detection using optical coherence tomography angiography: a pilot study. Br J Ophthalmol 102(11):1564–1569CrossRef
14.
go back to reference American Diabetes Association (2014) Diagnosis and classification of diabetes mellitus. Diabetes Care 37(Supplement 1):S81CrossRef American Diabetes Association (2014) Diagnosis and classification of diabetes mellitus. Diabetes Care 37(Supplement 1):S81CrossRef
15.
go back to reference Wilkinson CP, Ferris FL, Klein R, Lee PP, Agardh C, Davis MD, Dills DG, Kampik A, Pararajasegaram R, Verdaguer J (2003) Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology 110(9):1677–1682CrossRef Wilkinson CP, Ferris FL, Klein R, Lee PP, Agardh C, Davis MD, Dills DG, Kampik A, Pararajasegaram R, Verdaguer J (2003) Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology 110(9):1677–1682CrossRef
16.
go back to reference Kato K, Kondo M, Sugimoto M, Ikesugi K, Matsubara H (2015) Effect of pupil size on flicker ERGs recorded With RETeval system: new mydriasis-free full-field ERG system. Invest Ophthalmol Vis Sci 56(6):3684–3690CrossRef Kato K, Kondo M, Sugimoto M, Ikesugi K, Matsubara H (2015) Effect of pupil size on flicker ERGs recorded With RETeval system: new mydriasis-free full-field ERG system. Invest Ophthalmol Vis Sci 56(6):3684–3690CrossRef
17.
go back to reference Fukuo M, Kondo M, Hirose A, Fukushima H, Ikesugi K, Sugimoto M, Kato K, Uchigata Y, Kitano S (2016) Screening for diabetic retinopathy using new mydriasis-free, full-field flicker ERG recording device. Sci Rep 6(1):36591CrossRef Fukuo M, Kondo M, Hirose A, Fukushima H, Ikesugi K, Sugimoto M, Kato K, Uchigata Y, Kitano S (2016) Screening for diabetic retinopathy using new mydriasis-free, full-field flicker ERG recording device. Sci Rep 6(1):36591CrossRef
20.
go back to reference Arend O, Remky A, Evans D, Stuber R, Harris A (1997) Contrast sensitivity loss is coupled with capillary dropout in patients with diabetes. Invest Ophthalmol Vis Sci 38(9):1819–1824PubMed Arend O, Remky A, Evans D, Stuber R, Harris A (1997) Contrast sensitivity loss is coupled with capillary dropout in patients with diabetes. Invest Ophthalmol Vis Sci 38(9):1819–1824PubMed
21.
go back to reference Luu CD, Szental JA, Lee S, Lavanya R, Wong TY (2010) Correlation between retinal oscillatory potentials and retinal vascular caliber in type 2 diabetes. Invest Ophthalmol Vis Sci 51(1):482–486CrossRef Luu CD, Szental JA, Lee S, Lavanya R, Wong TY (2010) Correlation between retinal oscillatory potentials and retinal vascular caliber in type 2 diabetes. Invest Ophthalmol Vis Sci 51(1):482–486CrossRef
22.
go back to reference Kondo M, Sieving PA (2001) Primate photopic sine-wave flicker ERG: vector modeling analysis of component origins using glutamate analogs. Invest Ophthalmol Vis Sci 42(1):305–312PubMed Kondo M, Sieving PA (2001) Primate photopic sine-wave flicker ERG: vector modeling analysis of component origins using glutamate analogs. Invest Ophthalmol Vis Sci 42(1):305–312PubMed
23.
go back to reference Sapieha P (2012) Eyeing central neurons in vascular growth and reparative angiogenesis. Blood 120(11):2182–2194CrossRef Sapieha P (2012) Eyeing central neurons in vascular growth and reparative angiogenesis. Blood 120(11):2182–2194CrossRef
24.
go back to reference Moran EP, Wang Z, Chen J, Sapieha P, Smith LEH, Ma J (2016) Neurovascular cross talk in diabetic retinopathy: pathophysiological roles and therapeutic implications. Am J Physiol Heart Circ Physiol 311(3):H738–H749CrossRef Moran EP, Wang Z, Chen J, Sapieha P, Smith LEH, Ma J (2016) Neurovascular cross talk in diabetic retinopathy: pathophysiological roles and therapeutic implications. Am J Physiol Heart Circ Physiol 311(3):H738–H749CrossRef
25.
go back to reference Durbin MK, An L, Shemonski N, Soares M, Santos T, Lopes MC, Neves C, Cunhavaz J (2017) Quantification of retinal microvascular density in optical coherence tomographic angiography images in diabetic retinopathy. JAMA Ophthalmol 135(4):370–376CrossRef Durbin MK, An L, Shemonski N, Soares M, Santos T, Lopes MC, Neves C, Cunhavaz J (2017) Quantification of retinal microvascular density in optical coherence tomographic angiography images in diabetic retinopathy. JAMA Ophthalmol 135(4):370–376CrossRef
27.
go back to reference Tzekov R, Arden GB (1999) The electroretinogram in diabetic retinopathy. Surv Ophthalmol 44(1):53–60CrossRef Tzekov R, Arden GB (1999) The electroretinogram in diabetic retinopathy. Surv Ophthalmol 44(1):53–60CrossRef
28.
go back to reference Kooijman AC (1983) Light distribution on the retina of a wide-angle theoretical eye. J Opt Soc Am 73(11):1544–1550CrossRef Kooijman AC (1983) Light distribution on the retina of a wide-angle theoretical eye. J Opt Soc Am 73(11):1544–1550CrossRef
29.
go back to reference Pflibsen KP, Pomerantzeff O, Ross RN (1988) Retinal illuminance using a wide-angle model of the eye. J Opt Soc Am A Opt Image Sci Vis 5(1):146–150CrossRef Pflibsen KP, Pomerantzeff O, Ross RN (1988) Retinal illuminance using a wide-angle model of the eye. J Opt Soc Am A Opt Image Sci Vis 5(1):146–150CrossRef
30.
go back to reference Bedell HE, Katz LM (1982) On the necessity of correcting peripheral target luminance for pupillary area. Optom Vis Sci 59(10):767–769CrossRef Bedell HE, Katz LM (1982) On the necessity of correcting peripheral target luminance for pupillary area. Optom Vis Sci 59(10):767–769CrossRef
Metadata
Title
Retinal vasculature–function correlation in non-proliferative diabetic retinopathy
Authors
Yunkao Zeng
Dan Cao
Dawei Yang
Xuenan Zhuang
Yunyan Hu
Miao He
Honghua Yu
Jun Wang
Cheng Yang
Liang Zhang
Publication date
01-04-2020
Publisher
Springer Berlin Heidelberg
Published in
Documenta Ophthalmologica / Issue 2/2020
Print ISSN: 0012-4486
Electronic ISSN: 1573-2622
DOI
https://doi.org/10.1007/s10633-019-09724-4

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