Skip to main content
Top
Published in: Acta Diabetologica 7/2017

01-07-2017 | Original Article

Optical coherence tomography angiography analysis of retinal vascular plexuses and choriocapillaris in patients with type 1 diabetes without diabetic retinopathy

Authors: Adriano Carnevali, Riccardo Sacconi, Eleonora Corbelli, Livia Tomasso, Lea Querques, Gianpaolo Zerbini, Vincenzo Scorcia, Francesco Bandello, Giuseppe Querques

Published in: Acta Diabetologica | Issue 7/2017

Login to get access

Abstract

Aims

To analyze retinal vascular plexuses and choriocapillaris by optical coherence tomography angiography (OCT-A) and retinal nerve fiber layer and ganglion cell layer (GCL) by structural optical coherence tomography (OCT) in patients with type 1 diabetes mellitus (T1DM) without diabetic retinopathy (DR).

Methods

A total of 25 eyes of 25 consecutive T1DM patients without signs of DR were prospectively recruited and compared to 25 healthy subjects (control eyes). All patients underwent OCT-A (CIRRUS HD-OCT model 5000, Carl Zeiss Meditec, Dublin, CA) and structural OCT. Qualitative and quantitative analyses with vessel density were performed on OCT-A images in the superficial capillary plexus (SCP), deep capillary plexus (DCP) and choriocapillaris for all patients.

Results

By means of OCT-A, a rarefaction of the perifoveal capillary network in SCP was detected in 7 out of 25 eyes. No significant difference was found in FAZ area of both SCP and DCP comparing diabetic and control groups. By analyzing the DCP, diabetic eyes revealed a significant decreased vessel density compared to control eyes [0.464 ± 0.016 and 0.477 ± 0.014, respectively (p = 0.005)]. Instead, no significant difference was found in the vessel density of all-retina plexus, SCP and choriocapillaris. By RFNL and GCL thickness analysis, no significant differences were disclosed between diabetics and healthy subjects.

Conclusions

We demonstrated the ability of OCT-A to disclose early vascular alterations in patients with T1DM diagnosed as without any signs of DR on the basis of fundus biomicroscopy. Our results also suggest that microvascular changes could precede detectable damage of diabetic neuroretinopathy.
Literature
1.
go back to reference Prokofyeva E, Zrenner E (2012) Epidemiology of major eye diseases leading to blindness in Europe: a literature review. Ophthalmic Res 47:171–188CrossRefPubMed Prokofyeva E, Zrenner E (2012) Epidemiology of major eye diseases leading to blindness in Europe: a literature review. Ophthalmic Res 47:171–188CrossRefPubMed
2.
go back to reference Stewart MW (2016) Treatment of diabetic retinopathy: recent advances and unresolved challenges. World J Diabetes 25(7):333–341CrossRef Stewart MW (2016) Treatment of diabetic retinopathy: recent advances and unresolved challenges. World J Diabetes 25(7):333–341CrossRef
3.
go back to reference Lueder GT, Silverstein J (2005) Screening for retinopathy in the pediatric patient with type 1 diabetes mellitus. Pediatrics 116:270–273CrossRefPubMed Lueder GT, Silverstein J (2005) Screening for retinopathy in the pediatric patient with type 1 diabetes mellitus. Pediatrics 116:270–273CrossRefPubMed
4.
go back to reference Cho YH, Craig ME, Donaghue KC (2014) Puberty as an accelerator for diabetes complications. Pediatr Diabetes 15:18–26CrossRefPubMed Cho YH, Craig ME, Donaghue KC (2014) Puberty as an accelerator for diabetes complications. Pediatr Diabetes 15:18–26CrossRefPubMed
5.
go back to reference Fong DS, Aiello L, Gardner TW, American Diabetes Association et al (2003) Diabetic Retinopathy. Diabetes Care 26:226–229CrossRefPubMed Fong DS, Aiello L, Gardner TW, American Diabetes Association et al (2003) Diabetic Retinopathy. Diabetes Care 26:226–229CrossRefPubMed
9.
go back to reference Matsunaga DR, Yi JJ, De Koo LO, Ameri H, Puliafito CA, Kashani AH (2015) Optical coherence tomography angiography of diabetic retinopathy in human subjects. Ophthalmic Surg Lasers Imaging Retina 46:796–805CrossRefPubMed Matsunaga DR, Yi JJ, De Koo LO, Ameri H, Puliafito CA, Kashani AH (2015) Optical coherence tomography angiography of diabetic retinopathy in human subjects. Ophthalmic Surg Lasers Imaging Retina 46:796–805CrossRefPubMed
10.
go back to reference Kaidonis G, Gillies MC, Abhary S et al (2016) A single-nucleotide polymorphism in the MicroRNA-146a gene is associated with diabetic nephropathy and sight-threatening diabetic retinopathy in Caucasian patients. Acta Diabetol 53:643–650CrossRefPubMed Kaidonis G, Gillies MC, Abhary S et al (2016) A single-nucleotide polymorphism in the MicroRNA-146a gene is associated with diabetic nephropathy and sight-threatening diabetic retinopathy in Caucasian patients. Acta Diabetol 53:643–650CrossRefPubMed
11.
go back to reference Mazzeo A, Beltramo E, Iavello A, Carpanetto A, Porta M (2015) Molecular mechanisms of extracellular vesicle-induced vessel destabilization in diabetic retinopathy. Acta Diabetol 52:1113–1119CrossRefPubMed Mazzeo A, Beltramo E, Iavello A, Carpanetto A, Porta M (2015) Molecular mechanisms of extracellular vesicle-induced vessel destabilization in diabetic retinopathy. Acta Diabetol 52:1113–1119CrossRefPubMed
12.
go back to reference Rooney D, Lye WK, Tan G et al (2015) Body mass index and retinopathy in Asian populations with diabetes mellitus. Acta Diabetol 52:73–80CrossRefPubMed Rooney D, Lye WK, Tan G et al (2015) Body mass index and retinopathy in Asian populations with diabetes mellitus. Acta Diabetol 52:73–80CrossRefPubMed
13.
go back to reference Lu J, Hou X, Zhang L et al (2015) Association between body mass index and diabetic retinopathy in Chinese patients with type 2 diabetes. Acta Diabetol 52:701–708CrossRefPubMed Lu J, Hou X, Zhang L et al (2015) Association between body mass index and diabetic retinopathy in Chinese patients with type 2 diabetes. Acta Diabetol 52:701–708CrossRefPubMed
14.
go back to reference Beltramo E, Lopatina T, Mazzeo A et al (2016) Effects of the neuroprotective drugs somatostatin and brimonidine on retinal cell models of diabetic retinopathy. Acta Diabetol 53:957–964CrossRefPubMed Beltramo E, Lopatina T, Mazzeo A et al (2016) Effects of the neuroprotective drugs somatostatin and brimonidine on retinal cell models of diabetic retinopathy. Acta Diabetol 53:957–964CrossRefPubMed
15.
go back to reference El-Fayoumi D, Badr Eldine NM, Esmael AF, Ghalwash D, Soliman HM (2016) Retinal nerve fiber layer and ganglion cell complex thicknesses are reduced in children with type 1 diabetes with no evidence of vascular retinopathy. Invest Ophthalmol Vis Sci 57:5355–5360CrossRefPubMed El-Fayoumi D, Badr Eldine NM, Esmael AF, Ghalwash D, Soliman HM (2016) Retinal nerve fiber layer and ganglion cell complex thicknesses are reduced in children with type 1 diabetes with no evidence of vascular retinopathy. Invest Ophthalmol Vis Sci 57:5355–5360CrossRefPubMed
16.
go back to reference van Dijk HW, Verbraak FD, Kok PHB et al (2012) Early neurodegeneration in the retina of type 2 diabetic patients. Invest Ophthalmol Vis Sci 53:2715–2719CrossRefPubMedPubMedCentral van Dijk HW, Verbraak FD, Kok PHB et al (2012) Early neurodegeneration in the retina of type 2 diabetic patients. Invest Ophthalmol Vis Sci 53:2715–2719CrossRefPubMedPubMedCentral
17.
go back to reference Vujosevic S, Midena E (2013) Retinal layers changes in human preclinical and early clinical diabetic retinopathy support early retinal neuronal and Müller cells alterations. J Diabetes Res 90:50–58 Vujosevic S, Midena E (2013) Retinal layers changes in human preclinical and early clinical diabetic retinopathy support early retinal neuronal and Müller cells alterations. J Diabetes Res 90:50–58
19.
go back to reference De Benedetto U, Sacconi R, Pierro L, Lattanzio R, Bandello F (2015) Optical coherence tomographic hyperreflective foci in early stages of diabetic retinopathy. Retina 35:449–453CrossRefPubMed De Benedetto U, Sacconi R, Pierro L, Lattanzio R, Bandello F (2015) Optical coherence tomographic hyperreflective foci in early stages of diabetic retinopathy. Retina 35:449–453CrossRefPubMed
20.
go back to reference Bandello F, Corbelli E, Carnevali A, Pierro L, Querques G (2016) Optical coherence tomography angiography of diabetic retinopathy. Dev Ophthalmol 56:107–112CrossRefPubMed Bandello F, Corbelli E, Carnevali A, Pierro L, Querques G (2016) Optical coherence tomography angiography of diabetic retinopathy. Dev Ophthalmol 56:107–112CrossRefPubMed
21.
go back to reference Kim AY, Chu Z, Shahidzadeh A, Wang RK, Puliafito CA, Kashani AH (2016) Quantifying microvascular density and morphology in diabetic retinopathy using spectral-domain optical coherence tomography angiography. Invest Ophthalmol Vis Sci 57:362–370CrossRef Kim AY, Chu Z, Shahidzadeh A, Wang RK, Puliafito CA, Kashani AH (2016) Quantifying microvascular density and morphology in diabetic retinopathy using spectral-domain optical coherence tomography angiography. Invest Ophthalmol Vis Sci 57:362–370CrossRef
22.
go back to reference Dimitrova G, Chihara E, Takahashi H, Amano H, Okazaki K (2017) Quantitative retinal optical coherence tomography angiography in patients with diabetes without diabetic retinopathy. Invest Ophthalmol Vis Sci 58:190–196CrossRefPubMed Dimitrova G, Chihara E, Takahashi H, Amano H, Okazaki K (2017) Quantitative retinal optical coherence tomography angiography in patients with diabetes without diabetic retinopathy. Invest Ophthalmol Vis Sci 58:190–196CrossRefPubMed
23.
go back to reference Simonett JM, Scarinci F, Picconi F et al (2017) Early microvascular retinal changes in optical coherence tomography angiography in patients with type 1 diabetes mellitus. Acta Ophthalmol. doi:10.1111/aos.13404 PubMed Simonett JM, Scarinci F, Picconi F et al (2017) Early microvascular retinal changes in optical coherence tomography angiography in patients with type 1 diabetes mellitus. Acta Ophthalmol. doi:10.​1111/​aos.​13404 PubMed
25.
go back to reference Wang RK, Jacques S, Ma Z, Hurst S, Hanson S, Gruber A (2007) Three dimensional optical angiography. Opt Express 15:4083–4097CrossRefPubMed Wang RK, Jacques S, Ma Z, Hurst S, Hanson S, Gruber A (2007) Three dimensional optical angiography. Opt Express 15:4083–4097CrossRefPubMed
26.
go back to reference Wang RK (2010) Optical microangiography: a label free 3d imaging technology to visualize and quantify blood circulations within tissue beds in vivo. IEEE J Sel Top Quantum Electron 16:545–554CrossRefPubMedPubMedCentral Wang RK (2010) Optical microangiography: a label free 3d imaging technology to visualize and quantify blood circulations within tissue beds in vivo. IEEE J Sel Top Quantum Electron 16:545–554CrossRefPubMedPubMedCentral
27.
go back to reference An L, Wang RK (2008) In vivo volumetric imaging of vascular perfusion within human retina and choroids with optical micro-angiography. Opt Express 16:11438–11452CrossRefPubMed An L, Wang RK (2008) In vivo volumetric imaging of vascular perfusion within human retina and choroids with optical micro-angiography. Opt Express 16:11438–11452CrossRefPubMed
28.
go back to reference Samara WA, Say EA, Khoo CT et al (2015) Correlation of foveal avascular zone size with foveal morphology in normal eyes using optical coherence tomography angiography. Retina 35:2188–2195CrossRefPubMed Samara WA, Say EA, Khoo CT et al (2015) Correlation of foveal avascular zone size with foveal morphology in normal eyes using optical coherence tomography angiography. Retina 35:2188–2195CrossRefPubMed
29.
go back to reference Shahlaee A, Pefkianaki M, Hsu J, Ho AC (2016) Measurement of foveal avascular zone dimensions and its reliability in healthy eyes using optical coherence tomography angiography. Am J Ophthalmol 161(50–55):e51 Shahlaee A, Pefkianaki M, Hsu J, Ho AC (2016) Measurement of foveal avascular zone dimensions and its reliability in healthy eyes using optical coherence tomography angiography. Am J Ophthalmol 161(50–55):e51
30.
31.
go back to reference Battaglia Parodi M, Cicinelli MV, Rabiolo A, Pierro L, Bolognesi G, Bandello F (2016) Vascular abnormalities in patients with Stargardt disease assessed with optical coherence tomography angiography. Br J Ophthalmol. doi:10.1136/bjophthalmol-2016-308869 Battaglia Parodi M, Cicinelli MV, Rabiolo A, Pierro L, Bolognesi G, Bandello F (2016) Vascular abnormalities in patients with Stargardt disease assessed with optical coherence tomography angiography. Br J Ophthalmol. doi:10.​1136/​bjophthalmol-2016-308869
32.
go back to reference Scarinci F, Nesper PL, Fawzi AA (2016) Deep retinal capillary nonperfusion is associated with photoreceptor disruption in diabetic macular ischemia. Am J Ophthalmol 168:129–138CrossRefPubMed Scarinci F, Nesper PL, Fawzi AA (2016) Deep retinal capillary nonperfusion is associated with photoreceptor disruption in diabetic macular ischemia. Am J Ophthalmol 168:129–138CrossRefPubMed
33.
go back to reference Couturier A, Mané V, Bonnin S et al (2015) Capillary plexus anomalies in diabetic retinopathy on optical coherence tomography angiography. Retina 35:2384–2391CrossRefPubMed Couturier A, Mané V, Bonnin S et al (2015) Capillary plexus anomalies in diabetic retinopathy on optical coherence tomography angiography. Retina 35:2384–2391CrossRefPubMed
34.
go back to reference de Carlo TE, Chin AT, Bonini Filho MA et al (2015) Detection of microvascular changes in eyes of patients with diabetes but not clinical diabetic retinopathy using optical coherence tomography angiography. Retina 35:2364–2370CrossRefPubMed de Carlo TE, Chin AT, Bonini Filho MA et al (2015) Detection of microvascular changes in eyes of patients with diabetes but not clinical diabetic retinopathy using optical coherence tomography angiography. Retina 35:2364–2370CrossRefPubMed
35.
go back to reference Freiberg FJ, Pfau M, Wons J, Wirth MA, Becker MD, Michels S (2016) Optical coherence tomography angiography of the foveal avascular zone in diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol 254:1051–1058CrossRefPubMed Freiberg FJ, Pfau M, Wons J, Wirth MA, Becker MD, Michels S (2016) Optical coherence tomography angiography of the foveal avascular zone in diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol 254:1051–1058CrossRefPubMed
36.
go back to reference Arend O, Wolf S, Jung F et al (1991) Retinal microcirculation in patients with diabetes mellitus: dynamic and morphological analysis of perifoveal capillary network. Br J Ophthalmol 75:514–518CrossRefPubMedPubMedCentral Arend O, Wolf S, Jung F et al (1991) Retinal microcirculation in patients with diabetes mellitus: dynamic and morphological analysis of perifoveal capillary network. Br J Ophthalmol 75:514–518CrossRefPubMedPubMedCentral
37.
go back to reference Sander B, Larsen M, Engler C, Lund-Andersen H, Parving HH (1994) Early changes in diabetic retinopathy: capillary loss and blood-retina barrier permeability in relation to metabolic control. Acta Ophthalmol (Copenh) 72:553–559CrossRef Sander B, Larsen M, Engler C, Lund-Andersen H, Parving HH (1994) Early changes in diabetic retinopathy: capillary loss and blood-retina barrier permeability in relation to metabolic control. Acta Ophthalmol (Copenh) 72:553–559CrossRef
38.
go back to reference La Spina C, Carnevali A, Marchese A, Querques G, Bandello F (2016) Reproducibility and reliability of optical coherence tomography angiography for foveal avascular zone evaluation and measurement in different settings. Retina. doi:10.1097/IAE.0000000000001426 La Spina C, Carnevali A, Marchese A, Querques G, Bandello F (2016) Reproducibility and reliability of optical coherence tomography angiography for foveal avascular zone evaluation and measurement in different settings. Retina. doi:10.​1097/​IAE.​0000000000001426​
39.
go back to reference Reis A, Mateus C, Melo P, Figueira J, Cunha-Vaz J, Castelo-Branco M (2014) Neuroretinal dysfunction with intact blood-retinal barrier and absent vasculopathy in diabetes type 1. Diabetes 63:3926–3937CrossRefPubMed Reis A, Mateus C, Melo P, Figueira J, Cunha-Vaz J, Castelo-Branco M (2014) Neuroretinal dysfunction with intact blood-retinal barrier and absent vasculopathy in diabetes type 1. Diabetes 63:3926–3937CrossRefPubMed
40.
go back to reference Yoshida A, Kojima M, Ogasawara H, Ishiko S (1991) Oscillatory potentials and permeability of the blood-retinal barrier in noninsulin-dependent diabetic patients without retinopathy. Ophthalmology 98:1266–1271CrossRefPubMed Yoshida A, Kojima M, Ogasawara H, Ishiko S (1991) Oscillatory potentials and permeability of the blood-retinal barrier in noninsulin-dependent diabetic patients without retinopathy. Ophthalmology 98:1266–1271CrossRefPubMed
42.
go back to reference Rabiolo A, Carnevali A, Bandello F, Querques G (2016) Optical coherence tomography angiography: Evolution or revolution? expert. Rev of Ophthalmol 11:243–245CrossRef Rabiolo A, Carnevali A, Bandello F, Querques G (2016) Optical coherence tomography angiography: Evolution or revolution? expert. Rev of Ophthalmol 11:243–245CrossRef
Metadata
Title
Optical coherence tomography angiography analysis of retinal vascular plexuses and choriocapillaris in patients with type 1 diabetes without diabetic retinopathy
Authors
Adriano Carnevali
Riccardo Sacconi
Eleonora Corbelli
Livia Tomasso
Lea Querques
Gianpaolo Zerbini
Vincenzo Scorcia
Francesco Bandello
Giuseppe Querques
Publication date
01-07-2017
Publisher
Springer Milan
Published in
Acta Diabetologica / Issue 7/2017
Print ISSN: 0940-5429
Electronic ISSN: 1432-5233
DOI
https://doi.org/10.1007/s00592-017-0996-8

Other articles of this Issue 7/2017

Acta Diabetologica 7/2017 Go to the issue