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Published in: Japanese Journal of Ophthalmology 4/2020

01-07-2020 | Diabetic Retinopathy | Clinical Investigation

Ability of Swept source OCT technology to detect neurodegeneration in patients with type 2 diabetes mellitus without diabetic retinopathy

Authors: Maria Satue, Marta Cipres, Isabel Melchor, Laura Gil-Arribas, Elisa Vilades, Elena Garcia-Martin

Published in: Japanese Journal of Ophthalmology | Issue 4/2020

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Abstract

Purpose

To evaluate neurodegeneration in patients with type 2 Diabetes Mellitus (DM2) without diabetic retinopathy, and to assess the possible role of chronic systemic ischaemia and disease duration in retinal changes.

Study design

Observational cross sectional study.

Methods

Sixty eyes of 60 patients with DM2 without signs of diabetic retinopathy (DR), and 60 eyes of 60 healthy controls underwent retinal (ganglion cell layer (GCL), and retinal nerve fiber layer (RNFL) and choroidal evaluation using Swept source Optical coherence tomography, which allows high quality analysis of the different retinal layers and the choroidal plexus. Comparison between patients with presence/absence of systemic vascular complications and different disease duration time was performed.

Results

Macular GCL and RNFL were reduced in patients compared to controls (p < 0.001). In the peripapillary area, a reduction of the RNFL (p < 0.001) was observed in patients with DM2. There were no significant changes observed in the choroidal plexus of these patients. Patients with systemic ischaemia presented significant thinning of the choroid and further reduction of the temporal RNFL (p = 0.014) and GCL (p = 0.016) thickness. The GCL and the choroid were also thinner in patients with longer disease duration.

Conclusions

Patients with early DM2 present retinal neurodegeneration prior to the appearance of clinically observable vascular retinal changes. In these patients chronic systemic ischaemia caused reduction of the choroidal plexus and further damage to the retinal layers, adding new information on systemic chronic ischaemia and retinal neurodegeneration in patients with DM2 without DR.
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Literature
1.
go back to reference Santos AR, Ribeiro L, Bandello F, Lattanzio R, Egan C, Frydkjaer-Olsen U, et al. Functional and structural findings of neurodegeneration in early stages of diabetic retinopathy. Cross-sectional analyses of baseline data of the EUROCONDOR project. Diabetes. 2017;66:2503–10.CrossRef Santos AR, Ribeiro L, Bandello F, Lattanzio R, Egan C, Frydkjaer-Olsen U, et al. Functional and structural findings of neurodegeneration in early stages of diabetic retinopathy. Cross-sectional analyses of baseline data of the EUROCONDOR project. Diabetes. 2017;66:2503–10.CrossRef
2.
go back to reference Shahidi AM, Sampson GP, Pritchard N, Edwards K, Vagenas D, Russell AW, et al. Retinal nerve fibre layer thinning associated with diabetic peripheral neuropathy. Diabetes Med. 2012;29:e106–e111111.CrossRef Shahidi AM, Sampson GP, Pritchard N, Edwards K, Vagenas D, Russell AW, et al. Retinal nerve fibre layer thinning associated with diabetic peripheral neuropathy. Diabetes Med. 2012;29:e106–e111111.CrossRef
3.
go back to reference Salvi L, Plateroti P, Balducci S, Bollanti L, Conti FG, Vitale M, et al. Abnormalities of retinal ganglion cell complex at optical coherence tomography in patients with type 2 diabetes: a sign of diabetic polyneuropathy, not retinopathy. J Diabetes Complicat. 2016;30:469–76.CrossRef Salvi L, Plateroti P, Balducci S, Bollanti L, Conti FG, Vitale M, et al. Abnormalities of retinal ganglion cell complex at optical coherence tomography in patients with type 2 diabetes: a sign of diabetic polyneuropathy, not retinopathy. J Diabetes Complicat. 2016;30:469–76.CrossRef
4.
go back to reference Simó R, Hernández C. Neurodegeneration in the diabetic eye: new insights and therapeutic perspectives. Trends Endocrinol Metab. 2014;25:23–33. Simó R, Hernández C. Neurodegeneration in the diabetic eye: new insights and therapeutic perspectives. Trends Endocrinol Metab. 2014;25:23–33.
5.
go back to reference American Diabetes Association. Classification and diagnosis of diabetes. Diabetes Care. 2017;40(1):11–24.CrossRef American Diabetes Association. Classification and diagnosis of diabetes. Diabetes Care. 2017;40(1):11–24.CrossRef
6.
go back to reference Wilkinson CP, Ferris FL 3rd, Klein RE, Lee PP, Agardh CD, Davis M, et al. Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology. 2003;110:1677–82.CrossRef Wilkinson CP, Ferris FL 3rd, Klein RE, Lee PP, Agardh CD, Davis M, et al. Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology. 2003;110:1677–82.CrossRef
7.
go back to reference Satue M, Gavin A, Orduna E, Vilades E, Rodrigo MJ, Obis J, et al. Reproducibility and reliability of retinal and optic disc measurements obtained with swept-source optical coherence tomography in a healthy population. Jpn J Ophthalmol. 2019;63:165–71.CrossRef Satue M, Gavin A, Orduna E, Vilades E, Rodrigo MJ, Obis J, et al. Reproducibility and reliability of retinal and optic disc measurements obtained with swept-source optical coherence tomography in a healthy population. Jpn J Ophthalmol. 2019;63:165–71.CrossRef
8.
go back to reference Broe R, Rasmussen ML, Frydkjaer-Olsen U, Olsen BS, Mortensen HB, Hodgson L, et al. Retinal vessel calibers predict long-term microvascular complications in type 1 diabetes: The Danish cohort of pediatric diabetes 1987 (DCPD1987). Diabetes. 2014;63(11):3906–14.CrossRef Broe R, Rasmussen ML, Frydkjaer-Olsen U, Olsen BS, Mortensen HB, Hodgson L, et al. Retinal vessel calibers predict long-term microvascular complications in type 1 diabetes: The Danish cohort of pediatric diabetes 1987 (DCPD1987). Diabetes. 2014;63(11):3906–14.CrossRef
9.
go back to reference Cheung N, Rogers SL, Donaghue KC, Jenkins AJ, Tikellis G, Wong TY. Retinal arteriolar dilation predicts retinopathy in adolescents with type 1 diabetes. Diabetes Care. 2008;31:1842–6.CrossRef Cheung N, Rogers SL, Donaghue KC, Jenkins AJ, Tikellis G, Wong TY. Retinal arteriolar dilation predicts retinopathy in adolescents with type 1 diabetes. Diabetes Care. 2008;31:1842–6.CrossRef
10.
go back to reference Demirkaya N, van Dijk HW, van Schuppen SM, Abràmoff MD, Garvin MK, Sonka M, et al. Effect of age on individual retinal layer thickness in normal eyes as measured with spectral-domain optical coherence tomography. Investig Opthalmol Vis Sci. 2013;54:4934–40.CrossRef Demirkaya N, van Dijk HW, van Schuppen SM, Abràmoff MD, Garvin MK, Sonka M, et al. Effect of age on individual retinal layer thickness in normal eyes as measured with spectral-domain optical coherence tomography. Investig Opthalmol Vis Sci. 2013;54:4934–40.CrossRef
11.
go back to reference Sohn EH, van Dijk HW, Jiao C, Kok PHB, Jeong W, Demirkaya N, et al. Retinal neurodegeneration may precede microvascular changes characteristic of diabetic retinopathy in diabetes mellitus. Proc Natl Acad Sci USA. 2016;113(19):E2655–E26642664.CrossRef Sohn EH, van Dijk HW, Jiao C, Kok PHB, Jeong W, Demirkaya N, et al. Retinal neurodegeneration may precede microvascular changes characteristic of diabetic retinopathy in diabetes mellitus. Proc Natl Acad Sci USA. 2016;113(19):E2655–E26642664.CrossRef
12.
go back to reference Barber AJ. A new view of diabetic retinopathy: a neurodegenerative disease of the eye. Prog Neuropsychopharmacol Biol Psychiatry. 2003;27:283–90.CrossRef Barber AJ. A new view of diabetic retinopathy: a neurodegenerative disease of the eye. Prog Neuropsychopharmacol Biol Psychiatry. 2003;27:283–90.CrossRef
13.
go back to reference Valverde AM, Miranda S, García-Ramirez M, González-Rodriguez A, Hernández C, Simo R. Proapoptotic and survival signaling in the neuroretina at early stages of diabetic retinopathy. Mol Vis. 2013;19:47–53.PubMedPubMedCentral Valverde AM, Miranda S, García-Ramirez M, González-Rodriguez A, Hernández C, Simo R. Proapoptotic and survival signaling in the neuroretina at early stages of diabetic retinopathy. Mol Vis. 2013;19:47–53.PubMedPubMedCentral
14.
go back to reference Van Dijk HW, Verbraak FD, Kok PH, Garvin MK, Sonka M, Lee K, et al. Decreased retinal ganglion cell layer thickness in type 1 diabetic patients. Invest Ophthalmol Vis Sci. 2010;51:3660–5.CrossRef Van Dijk HW, Verbraak FD, Kok PH, Garvin MK, Sonka M, Lee K, et al. Decreased retinal ganglion cell layer thickness in type 1 diabetic patients. Invest Ophthalmol Vis Sci. 2010;51:3660–5.CrossRef
15.
go back to reference Van Dijk HW, Verbraak FD, Stehouwer M, Kok PHB, Garvin MK, Sonka M, et al. Association of visual function and ganglion cell layer thickness in patients with diabetes mellitus type 1 and no or minimal diabetic retinopathy. Vision Res. 2011;51:224–8.CrossRef Van Dijk HW, Verbraak FD, Stehouwer M, Kok PHB, Garvin MK, Sonka M, et al. Association of visual function and ganglion cell layer thickness in patients with diabetes mellitus type 1 and no or minimal diabetic retinopathy. Vision Res. 2011;51:224–8.CrossRef
16.
go back to reference Bringmann A, Wiedemann P. Müller glial cells in retinal disease. Ophthalmologica. 2012;227:1–19.CrossRef Bringmann A, Wiedemann P. Müller glial cells in retinal disease. Ophthalmologica. 2012;227:1–19.CrossRef
17.
go back to reference Vujosevic S, Midena E. Retinal layers changes in human preclinical and early clinical diabetic retinopathy support early retinal neuronal and Müller cells alterations. J Diabetes Res. 2013;2013:905058.PubMedPubMedCentral Vujosevic S, Midena E. Retinal layers changes in human preclinical and early clinical diabetic retinopathy support early retinal neuronal and Müller cells alterations. J Diabetes Res. 2013;2013:905058.PubMedPubMedCentral
18.
go back to reference Zhu T, Ma J, Li Y, Zhang Z. Association between retinal neuronal degeneration and visual function impairment in type 2 diabetic patients without diabetic retinopathy. Sci China Life Sci. 2015;58:550–5.CrossRef Zhu T, Ma J, Li Y, Zhang Z. Association between retinal neuronal degeneration and visual function impairment in type 2 diabetic patients without diabetic retinopathy. Sci China Life Sci. 2015;58:550–5.CrossRef
19.
go back to reference De Clerck EEB, Schouten JSAG, Berendschot TTJM, Kessels AGH, Nuijts RMMA, Beckers HJM, et al. New ophthalmologic imaging techniques for detection and monitoring of neurodegenerative changes in diabetes: a systematic review. Lancet Diabetes Endocrinol. 2015;3:653–63.CrossRef De Clerck EEB, Schouten JSAG, Berendschot TTJM, Kessels AGH, Nuijts RMMA, Beckers HJM, et al. New ophthalmologic imaging techniques for detection and monitoring of neurodegenerative changes in diabetes: a systematic review. Lancet Diabetes Endocrinol. 2015;3:653–63.CrossRef
20.
go back to reference Sánchez-Tocino H, Alvarez-Vidal A, Maldonado MJ, Moreno-Montañés J, García-Layana A, Moreno-Montañés J, et al. retinal thickness study with optical coherence tomography in patients with diabetes. Invest Ophthalmol Vis Sci. 2002;43:1588–94.PubMed Sánchez-Tocino H, Alvarez-Vidal A, Maldonado MJ, Moreno-Montañés J, García-Layana A, Moreno-Montañés J, et al. retinal thickness study with optical coherence tomography in patients with diabetes. Invest Ophthalmol Vis Sci. 2002;43:1588–94.PubMed
21.
go back to reference Asefzadeh B, Fisch BM, Parenteau CE, Cavallerano AA. Macular thickness and systemic markers for diabetes in individuals with no or mild diabetic retinopathy. Clin Exp Ophthalmol. 2008;36:455–63.CrossRef Asefzadeh B, Fisch BM, Parenteau CE, Cavallerano AA. Macular thickness and systemic markers for diabetes in individuals with no or mild diabetic retinopathy. Clin Exp Ophthalmol. 2008;36:455–63.CrossRef
22.
go back to reference Chen Y, Li J, Yan Y, Shen X. Diabetic macular morphology changes may occur in the early stage of diabetes. BMC Ophthalmol. 2016;16:12.CrossRef Chen Y, Li J, Yan Y, Shen X. Diabetic macular morphology changes may occur in the early stage of diabetes. BMC Ophthalmol. 2016;16:12.CrossRef
23.
go back to reference Bronson-Castain KW, Bearse MA, Neuville J, Jonasdottir S, King-Hooper B, Barez S, et al. Adolescents with Type 2 diabetes: early indications of focal retinal neuropathy, retinal thinning, and venular dilation. Retina. 2009;29:618–26.CrossRef Bronson-Castain KW, Bearse MA, Neuville J, Jonasdottir S, King-Hooper B, Barez S, et al. Adolescents with Type 2 diabetes: early indications of focal retinal neuropathy, retinal thinning, and venular dilation. Retina. 2009;29:618–26.CrossRef
24.
go back to reference Verma A, Rani PK, Raman R, Pal SS, Laxmi G, Gupta M, et al. Is neuronal dysfunction an early sign of diabetic retinopathy? Microperimetry and spectral domain optical coherence tomography (SD-OCT) study in individuals with diabetes, but no diabetic retinopathy. Eye. 2009;23:1824–30.CrossRef Verma A, Rani PK, Raman R, Pal SS, Laxmi G, Gupta M, et al. Is neuronal dysfunction an early sign of diabetic retinopathy? Microperimetry and spectral domain optical coherence tomography (SD-OCT) study in individuals with diabetes, but no diabetic retinopathy. Eye. 2009;23:1824–30.CrossRef
25.
go back to reference Oshitari T, Hanawa K, Adachi-Usami E. Changes of macular and RNFL thicknesses measured by Stratus OCT in patients with early stage diabetes. Eye (London). 2009;23:884–9.CrossRef Oshitari T, Hanawa K, Adachi-Usami E. Changes of macular and RNFL thicknesses measured by Stratus OCT in patients with early stage diabetes. Eye (London). 2009;23:884–9.CrossRef
26.
go back to reference Araszkiewicz A, Zozulińska-Ziółkiewicz D, Meller M, Bernardczyk-Meller J, Piłaciński S, Rogowicz-Frontczak A, et al. Neurodegeneration of the retina in type 1 diabetic patients. Polish Arch Intern Med. 2012;122:464–70.CrossRef Araszkiewicz A, Zozulińska-Ziółkiewicz D, Meller M, Bernardczyk-Meller J, Piłaciński S, Rogowicz-Frontczak A, et al. Neurodegeneration of the retina in type 1 diabetic patients. Polish Arch Intern Med. 2012;122:464–70.CrossRef
27.
go back to reference Cabrera DeBuc D, Somfai GM. Early detection of retinal thickness changes in diabetes using Optical Coherence Tomography. Med Sci Monit. 2010;16:15–211. Cabrera DeBuc D, Somfai GM. Early detection of retinal thickness changes in diabetes using Optical Coherence Tomography. Med Sci Monit. 2010;16:15–211.
28.
go back to reference Scarinci F, Picconi F, Virgili G, Giorno P, Di Renzo A, Varano M, et al. Single retinal layer evaluation in patients with type 1 diabetes with no or early signs of diabetic retinopathy: the first hint of neurovascular crosstalk damage between neurons and capillaries? Ophthalmologica. 2017;237:223–31.CrossRef Scarinci F, Picconi F, Virgili G, Giorno P, Di Renzo A, Varano M, et al. Single retinal layer evaluation in patients with type 1 diabetes with no or early signs of diabetic retinopathy: the first hint of neurovascular crosstalk damage between neurons and capillaries? Ophthalmologica. 2017;237:223–31.CrossRef
29.
go back to reference Gundogan FC, Akay F, Uzun S, Yolcu U, Çağıltay E, Toyran S. Early neurodegeneration of the inner retinal layers in type 1 diabetes mellitus. Ophthalmologica. 2015;235:125–32.CrossRef Gundogan FC, Akay F, Uzun S, Yolcu U, Çağıltay E, Toyran S. Early neurodegeneration of the inner retinal layers in type 1 diabetes mellitus. Ophthalmologica. 2015;235:125–32.CrossRef
30.
go back to reference Ng DS, Chiang PP, Tan G, Cheung C, Cheng C-Y, Cheung CY, et al. Retinal ganglion cell neuronal damage in diabetes and diabetic retinopathy. Clin Exp Ophthalmol. 2016;44:243–50.CrossRef Ng DS, Chiang PP, Tan G, Cheung C, Cheng C-Y, Cheung CY, et al. Retinal ganglion cell neuronal damage in diabetes and diabetic retinopathy. Clin Exp Ophthalmol. 2016;44:243–50.CrossRef
31.
go back to reference Sugimoto M, Sasoh M, Ido M, Wakitani Y, Takahashi C, Uji Y. Detection of early diabetic change with optical coherence tomography in type 2 diabetes mellitus patients without retinopathy. Ophthalmologica. 2005;219:379–85.CrossRef Sugimoto M, Sasoh M, Ido M, Wakitani Y, Takahashi C, Uji Y. Detection of early diabetic change with optical coherence tomography in type 2 diabetes mellitus patients without retinopathy. Ophthalmologica. 2005;219:379–85.CrossRef
32.
go back to reference Verma A, Raman R, Vaitheeswaran K, Pal SS, Laxmi G, Gupta M, et al. Does neuronal damage precede vascular damage in subjects with type 2 diabetes mellitus and having no clinical diabetic retinopathy? Ophthalmic Res. 2012;47:202–7.CrossRef Verma A, Raman R, Vaitheeswaran K, Pal SS, Laxmi G, Gupta M, et al. Does neuronal damage precede vascular damage in subjects with type 2 diabetes mellitus and having no clinical diabetic retinopathy? Ophthalmic Res. 2012;47:202–7.CrossRef
33.
go back to reference Carpineto P, Toto L, Aloia R, Ciciarelli V, Borrelli E, Vitacolonna E, et al. Neuroretinal alterations in the early stages of diabetic retinopathy in patients with type 2 diabetes mellitus. Eye (London). 2016;30:673–9.CrossRef Carpineto P, Toto L, Aloia R, Ciciarelli V, Borrelli E, Vitacolonna E, et al. Neuroretinal alterations in the early stages of diabetic retinopathy in patients with type 2 diabetes mellitus. Eye (London). 2016;30:673–9.CrossRef
Metadata
Title
Ability of Swept source OCT technology to detect neurodegeneration in patients with type 2 diabetes mellitus without diabetic retinopathy
Authors
Maria Satue
Marta Cipres
Isabel Melchor
Laura Gil-Arribas
Elisa Vilades
Elena Garcia-Martin
Publication date
01-07-2020
Publisher
Springer Japan
Published in
Japanese Journal of Ophthalmology / Issue 4/2020
Print ISSN: 0021-5155
Electronic ISSN: 1613-2246
DOI
https://doi.org/10.1007/s10384-020-00729-0

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