The aim of this narrative mini review is to analyze optical coherence tomography angiography (OCTA) parameters from reports that involved both superficial and deep vascular layers in patients with diabetes and to assess their relevance for the pathogenesis of diabetic retinopathy (DR). Papers published from January 2015 to August 2018 describing the use of OCTA in diabetes were identified and reviewed through a Medline/PubMed search. OCTA studies suggest that parameters are altered in patients with diabetes in all retinal vascular layers. From all included studies that evaluated both the superficial and the deep vascular layer, a number of studies suggested that the deep vascular layer was affected at an earlier stage of DR. OCTA parameter alterations were more prominent in the deep vascular layer than in the superficial vascular layer in patients with DR, and deep-vascular-layer alterations were most evident in patients with diabetic macular edema. Regarding that retinal venules originate from the deep vascular layer of the retina, alteration of OCTA parameters at the deep vascular layer in diabetic patients may imply a predominant affection of the venous side of the retinal vascular system in the pathogenesis of DR.

1.
Flaxman
SR
,
Bourne
RR
,
Resnikoff
S
,
Ackland
P
,
Braithwaite
T
,
Cicinelli
MV
, et al.;
Vision Loss Expert Group of the Global Burden of Disease Study
.
Global causes of blindness and distance vision impairment 1990-2020: a systematic review and meta-analysis
.
Lancet Glob Health
.
2017
Dec
;
5
(
12
):
e1221
34
.
[PubMed]
2214-109X
2.
Pemp
B
,
Polska
E
,
Garhofer
G
,
Bayerle-Eder
M
,
Kautzky-Willer
A
,
Schmetterer
L
.
Retinal blood flow in type 1 diabetic patients with no or mild diabetic retinopathy during euglycemic clamp
.
Diabetes Care
.
2010
Sep
;
33
(
9
):
2038
42
.
[PubMed]
0149-5992
3.
Spaide
RF
,
Fujimoto
JG
,
Waheed
NK
,
Sadda
SR
,
Staurenghi
G
.
Optical coherence tomography angiography
.
Prog Retin Eye Res
.
2018
May
;
64
:
1
55
.
[PubMed]
1350-9462
4.
Hasegawa
N
,
Nozaki
M
,
Takase
N
,
Yoshida
M
,
Ogura
Y
.
New Insights Into Microaneurysms in the Deep Capillary Plexus Detected by Optical Coherence Tomography Angiography in Diabetic Macular Edema
.
Invest Ophthalmol Vis Sci
.
2016
Jul
;
57
(
9
):
OCT348
55
.
[PubMed]
0146-0404
5.
Choi
W
,
Waheed
NK
,
Moult
EM
,
Adhi
M
,
Lee
B
,
De Carlo
T
, et al.
Ultrahigh speed swept source optical coherence tomography angiography of retinal and choriocapillaris alterations in diabetic patients with and without retinopathy
.
Retina
.
2017
Jan
;
37
(
1
):
11
21
.
[PubMed]
0275-004X
6.
Vujosevic
S
,
Muraca
A
,
Alkabes
M
,
Villani
E
,
Cavarzeran
F
,
Rossetti
L
, et al.
De Cillaʼ S. Early microvascular and neural changes in patients with type 1 and type 2 diabetes mellitus without clinical signs of diabetic retinopathy
.
Retina
.
2017
Dec
;
•••
:
1
.
[PubMed]
0275-004X
7.
Dimitrova
G
,
Chihara
E
,
Takahashi
H
,
Amano
H
,
Okazaki
K
.
Quantitative Retinal Optical Coherence Tomography Angiography in Patients With Diabetes Without Diabetic Retinopathy
.
Invest Ophthalmol Vis Sci
.
2017
Jan
;
58
(
1
):
190
6
.
[PubMed]
0146-0404
8.
Takase
N
,
Nozaki
M
,
Kato
A
,
Ozeki
H
,
Yoshida
M
,
Ogura
Y
.
Enlargement of foveal avascular zone in diabetic eyes evaluated by en face optical coherence tomography angiography
.
Retina
.
2015
Nov
;
35
(
11
):
2377
83
.
[PubMed]
0275-004X
9.
Cao
D
,
Yang
D
,
Huang
Z
,
Zeng
Y
,
Wang
J
,
Hu
Y
, et al.
Optical coherence tomography angiography discerns preclinical diabetic retinopathy in eyes of patients with type 2 diabetes without clinical diabetic retinopathy
.
Acta Diabetol
.
2018
May
;
55
(
5
):
469
77
.
[PubMed]
0940-5429
10.
Scarinci
F
,
Picconi
F
,
Giorno
P
,
Boccassini
B
,
De Geronimo
D
,
Varano
M
, et al.
Deep capillary plexus impairment in patients with type 1 diabetes mellitus with no signs of diabetic retinopathy revealed using optical coherence tomography angiography
.
Acta Ophthalmol
.
2018
Mar
;
96
(
2
):
e264
5
.
[PubMed]
1755-375X
11.
Carnevali
A
,
Sacconi
R
,
Corbelli
E
,
Tomasso
L
,
Querques
L
,
Zerbini
G
, et al.
Optical coherence tomography angiography analysis of retinal vascular plexuses and choriocapillaris in patients with type 1 diabetes without diabetic retinopathy
.
Acta Diabetol
.
2017
Jul
;
54
(
7
):
695
702
.
[PubMed]
0940-5429
12.
Meshi
A
,
Chen
KC
,
You
QS
,
Dans
K
,
Lin
T
,
Bartsch
DU
, et al.
ANATOMICAL AND FUNCTIONAL TESTING IN DIABETIC PATIENTS WITHOUT RETINOPATHY: Results of Optical Coherence Tomography Angiography and Visual Acuity Under Varying Contrast and Luminance Conditions
.
Retina
.
2018
Jul
;
•••
:
[PubMed]
0275-004X
13.
Chen
Q
,
Ma
Q
,
Wu
C
,
Tan
F
,
Chen
F
,
Wu
Q
, et al.
Macular Vascular Fractal Dimension in the Deep Capillary Layer as an Early Indicator of Microvascular Loss for Retinopathy in Type 2 Diabetic Patients
.
Invest Ophthalmol Vis Sci
.
2017
Jul
;
58
(
9
):
3785
94
.
[PubMed]
0146-0404
14.
Salz
DA
,
de Carlo
TE
,
Adhi
M
,
Moult
E
,
Choi
W
,
Baumal
CR
, et al.
Select Features of Diabetic Retinopathy on Swept-Source Optical Coherence Tomographic Angiography Compared With Fluorescein Angiography and Normal Eyes
.
JAMA Ophthalmol
.
2016
Jun
;
134
(
6
):
644
50
.
[PubMed]
2168-6165
15.
Ishibazawa
A
,
Nagaoka
T
,
Takahashi
A
,
Omae
T
,
Tani
T
,
Sogawa
K
, et al.
Optical Coherence Tomography Angiography in Diabetic Retinopathy: A Prospective Pilot Study
.
Am J Ophthalmol
.
2015
Jul
;
160
(
1
):
35
44.e1
.
[PubMed]
0002-9394
16.
Couturier
A
,
Mané
V
,
Bonnin
S
,
Erginay
A
,
Massin
P
,
Gaudric
A
, et al.
Capillary plexus anomalies in diabetic retinopathy on optical coherence tomography angiography
.
Retina
.
2015
Nov
;
35
(
11
):
2384
91
.
[PubMed]
0275-004X
17.
Mastropasqua
R
,
Toto
L
,
Mastropasqua
A
,
Aloia
R
,
De Nicola
C
,
Mattei
PA
, et al.
Foveal avascular zone area and parafoveal vessel density measurements in different stages of diabetic retinopathy by optical coherence tomography angiography
.
Int J Ophthalmol
.
2017
Oct
;
10
(
10
):
1545
51
.
[PubMed]
2222-3959
18.
Freiberg
FJ
,
Pfau
M
,
Wons
J
,
Wirth
MA
,
Becker
MD
,
Michels
S
.
Optical coherence tomography angiography of the foveal avascular zone in diabetic retinopathy
.
Graefes Arch Clin Exp Ophthalmol
.
2016
Jun
;
254
(
6
):
1051
8
.
[PubMed]
0721-832X
19.
Gozlan
J
,
Ingrand
P
,
Lichtwitz
O
,
Cazet-Supervielle
A
,
Benoudis
L
,
Boissonnot
M
, et al.
Retinal microvascular alterations related to diabetes assessed by optical coherence tomography angiography: A cross-sectional analysis
.
Medicine (Baltimore)
.
2017
Apr
;
96
(
15
):
e6427
.
[PubMed]
0025-7974
20.
Al-Sheikh
M
,
Akil
H
,
Pfau
M
,
Sadda
SR
.
Swept-Source OCT Angiography Imaging of the Foveal Avascular Zone and Macular Capillary Network Density in Diabetic Retinopathy
.
Invest Ophthalmol Vis Sci
.
2016
Jul
;
57
(
8
):
3907
13
.
[PubMed]
0146-0404
21.
Simonett
JM
,
Scarinci
F
,
Picconi
F
,
Giorno
P
,
De Geronimo
D
,
Di Renzo
A
, et al.
Early microvascular retinal changes in optical coherence tomography angiography in patients with type 1 diabetes mellitus
.
Acta Ophthalmol
.
2017
Dec
;
95
(
8
):
e751
5
.
[PubMed]
1755-375X
22.
Nesper
PL
,
Roberts
PK
,
Onishi
AC
,
Chai
H
,
Liu
L
,
Jampol
LM
, et al.
Quantifying Microvascular Abnormalities With Increasing Severity of Diabetic Retinopathy Using Optical Coherence Tomography Angiography
.
Invest Ophthalmol Vis Sci
.
2017
May
;
58
(
6
):
BIO307
15
.
[PubMed]
0146-0404
23.
Sambhav
K
,
Abu-Amero
KK
,
Chalam
KV
.
Deep capillary macular perfusion indices obtained with OCT angiography correlate with degree of nonproliferative diabetic retinopathy
.
Eur J Ophthalmol
.
2017
Nov
;
27
(
6
):
716
29
.
[PubMed]
1120-6721
24.
Ting
DS
,
Tan
GS
,
Agrawal
R
,
Yanagi
Y
,
Sie
NM
,
Wong
CW
, et al.
Optical Coherence Tomographic Angiography in Type 2 Diabetes and Diabetic Retinopathy
.
JAMA Ophthalmol
.
2017
Apr
;
135
(
4
):
306
12
.
[PubMed]
2168-6165
25.
Zahid
S
,
Dolz-Marco
R
,
Freund
KB
,
Balaratnasingam
C
,
Dansingani
K
,
Gilani
F
,
Mehta
N
,
Young
E
,
Klifto
MR
,
Chae
B
,
Yannuzzi
LA
,
Young
JA
. Fractal Dimensional Analysis of Optical Coherence Tomography Angiography in Eyes With Diabetic Retinopathy. 6-19656.
26.
Dupas
B
,
Minvielle
W
,
Bonnin
S
,
Couturier
A
,
Erginay
A
,
Massin
P
, et al.
Association Between Vessel Density and Visual Acuity in Patients With Diabetic Retinopathy and Poorly Controlled Type 1 Diabetes
.
JAMA Ophthalmol
.
2018
Jul
;
136
(
7
):
721
8
.
[PubMed]
2168-6165
27.
Bhardwaj
S
,
Tsui
E
,
Zahid
S
,
Young
E
,
Mehta
N
,
Agemy
S
, et al.
Value of fractal analysis of optical coherence tomography angiography in various stages of diabetic retinpathy
.
Retina
.
2017
Jul
;
•••
:
[PubMed]
0275-004X
28.
Krawitz
BD
,
Mo
S
,
Geyman
LS
,
Agemy
SA
,
Scripsema
NK
,
Garcia
PM
, et al.
Acircularity index and axis ratio of the foveal avascular zone in diabetic eyes and healthy controls measured by optical coherence tomography angiography
.
Vision Res
.
2017
Oct
;
139
:
177
86
.
[PubMed]
0042-6989
29.
Mané
V
,
Dupas
B
,
Gaudric
A
,
Bonnin
S
,
Pedinielli
A
,
Bousquet
E
, et al.
Correlation between cystoids spaces in chronic diabetic macular edema and capillary nonperfusion detected by optical coherence tomography angiography
.
Retina
.
2016
Dec
;
36
Suppl 1
:
S102
10
.
[PubMed]
0275-004X
30.
Toto
L
,
D’Aloisio
R
,
Di Nicola
M
,
Di Martino
G
,
Di Staso
S
,
Ciancaglini
M
, et al.
Qualitative and Quantitative Assessment of Vascular Changes in Diabetic Macular Edema after Dexamethasone Implant Using Optical Coherence Tomography Angiography
.
Int J Mol Sci
.
2017
Jun
;
18
(
6
):
E1181
.
[PubMed]
1661-6596
31.
Lee
J
,
Moon
BG
,
Cho
AR
,
Yoon
YH
.
Optical Coherence Tomography Angiography of DME and Its Association with Anti-VEGF Treatment Response
.
Ophthalmology
.
2016
Nov
;
123
(
11
):
2368
75
.
[PubMed]
0161-6420
32.
Dodo
Y
,
Murakami
T
,
Suzuma
K
,
Yoshitake
S
,
Yoshitake
T
,
Ishihara
K
, et al.
Diabetic Neuroglial Changes in the Superficial and Deep Nonperfused Areas on Optical Coherence Tomography Angiography
.
Invest Ophthalmol Vis Sci
.
2017
Nov
;
58
(
13
):
5870
9
.
[PubMed]
0146-0404
33.
Park
JJ
,
Soetikno
BT
,
Fawzi
AA
.
Characterization of the middle capillary plexus using optical coherence tomography angiography in healthy and diabetic eyes
.
Retina
.
2016
Nov
;
36
(
11
):
2039
50
.
[PubMed]
0275-004X
34.
Klein
R
,
Myers
CE
,
Lee
KE
,
Gangnon
R
,
Klein
BE
.
Changes in retinal vessel diameter and incidence and progression of diabetic retinopathy
.
Arch Ophthalmol
.
2012
Jun
;
130
(
6
):
749
55
.
[PubMed]
0003-9950
35.
Dimitrova
G
,
Kato
S
,
Yamashita
H
,
Tamaki
Y
,
Nagahara
M
,
Fukushima
H
, et al.
Relation between retrobulbar circulation and progression of diabetic retinopathy
.
Br J Ophthalmol
.
2003
May
;
87
(
5
):
622
5
.
[PubMed]
0007-1161
36.
Cybulska-Heinrich
AK
,
Baertschi
M
,
Loesche
CC
,
Schoetzau
A
,
Konieczka
K
,
Josifova
T
, et al.
Patients with diabetic retinopathy have high retinal venous pressure
.
EPMA J
.
2015
Feb
;
6
(
1
):
5
.
[PubMed]
1878-5077
37.
Bek
T
. Histopathology and pathophysiology of diabetic retinopathy. In:
van Bijsterveld
OP
, editor
.
Diabetic retinopathy
.
London
:
Martin Dunitz
;
2000
. pp.
169
89
.
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