Structural and functional retinal changes in patients with type 2 diabetes without diabetic retinopathy

Figures & data

Figure 1. Diagram of the ETDRS chart. The retinal sensitivity test results of microperimetry are automatically matched with the fundus photos. (A) Right eye; (B) Left eye.

Figure 2. OCTA scans. (A) The superficial capillary plexus; (B) deep capillary plexus; (C) radial peripapillary capillary plexus.

Table 1. Characteristics of the participants.

Characteristics	NDR (n = 34)	Control (n = 37)	p
Sex, n (%)			.119
Male	21 (61.8%)	16 (43.2%)
Female	13 (38.2%)	21 (56.8%)
Age (years), median (P25, P75)	54.5 (50, 62)	53 (48, 57)	.302
BMI (kg/m^2), mean ± SD	25.2 ± 2.4	24.6 ± 2.0	.235
SBP (mmHg), mean ± SD	124 ± 11	121 ± 9	.249
DBP (mmHg), mean ± SD	77 ± 8	76 ± 6	.521
TG (mmol/L), median (P25, P75)	1.44 (1.01, 2.2)	1.23 (0.98, 1.67)	.236
TC (mmol/L), mean ± SD	4.41 ± 0.820	4.37 ± 0.562	.802
HDL (mmol/L), mean ± SD	1.41 ± 0.270	1.43 ± 0.241	.816
LDL (mmol/L), mean ± SD	2.72 ± 0.719	2.82 ± 0.416	.481
Serum urea (mmol/L), median (P25, P75)	5.05 (4.5, 5.9)	5.02 (4.74, 5.36)	.791
Serum creatinine (μmol/L)	64.81 ± 11.005	68.34 ± 8.674	.136
BCVA (LogMAR), median (P25, P75)	0.00 (0.00, 0.10)	0.00 (0.00, 0.00)	.138
IOP (mmHg), mean ± SD	16.07 ± 2.04	15.38 ± 2.06	.102
Duration of diabetes (years)	8.6 ± 5.38	–	–
HbA1c (%), median (P25, P75)	7.05 (6.1, 8.6)	–	–
Metformin/acarbose/glimepiride, n (%)	21 (61.8)	–	–
Insulin aspart/insulin glargine, n (%)	5 (14.7)	–	–
Acarbose and insulin glargine, n (%)	8 (23.5)	–	–

NDR: diabetic patients without diabetic retinopathy; BMI: body mass index; SBP: systolic blood pressure; DBP: diastolic blood pressure; TG: triglyceride; TC: total cholesterol; HDL: high-density lipoprotein; LDL: low-density lipoprotein; BCVA: best-corrected visual acuity; IOP: intraocular pressure; HbA1c: glycated haemoglobin.

Table 2. Microperimetric retinal sensitivity (dB).

ETDRS sectors	NDR (n = 51)	Control (n = 49)	p^a
S	24.97 ± 1.14	26.40 ± 1.30	<.001
S1	25.38 ± 1.79	27.63 ± 1.19	<.001
S2	24.03 ± 1.32	25.53 ± 1.42	<.001
T	25.71 ± 1.31	27.49 ± 1.16	<.001
T1	26.34 ± 1.56	28.51 ± 1.19	<.001
T2	25.45 ± 1.32	26.72 ± 1.26	<.001
I	25.09 ± 1.00	26.62 ± 1.47	<.001
I1	26.15 ± 1.10	27.96 ± 1.33	<.001
I2	24.13 ± 1.36	25.80 ± 1.66	<.001
N	24.73 ± 1.26	26.33 ± 1.14	<.001
N1	26.37 ± 1.17	28.18 ± 1.28	<.001
N2	24.06 ± 1.09	25.26 ± 1.36	<.001
M	27.02 ± 1.17	29.07 ± 1.15	<.001

ETDRS: Early Treatment of Diabetic Retinopathy Study; NDR: diabetic patients without diabetic retinopathy; S: superior; T: temporal; I: inferior; N: nasal; M: middle.

^aThe p-values were adjusted for multiple comparisons using the Holm–Bonferroni method.

Table 3. Microvascular changes, VD and PD of RPCP, SCP, and DCP, and FAZ area, perimeter, and circularity.

Parameters	NDR (n = 51)	Control (n = 49)	p
Capillary drop-out, n (%)	40(78.4)	26(53.1)	.007
Notched or punched out borders, n (%)	44(86.3)	20(40.8)	<.001
Loss of smooth contour, n (%)	41(80.4)	13(26.5)	<.001
Cross vessel, n (%)	3(5.9)	0	.243*
VD of RPCP (%)
T	21.41 ± 3.56	20.43 ± 2.95	.177#
S	22.20 ± 2.99	20.16 ± 2.27	<.001
N	21.20 ± 3.53	17.63 ± 2.33	<.001
I	20.98 ± 3.73	18.90 ± 2.31	.001
PD of RPCP (%)
T	96.78 ± 10.82	101.71 ± 15.40	.030#
S	110.22 ± 7.33	105.51 ± 7.53	.002
N	101.53 ± 10.39	93.55 ± 10.42	<.001
I	103.61 ± 11.66	103.18 ± 9.88	.986#
FAZ
Area (mm^2)	0.34 ± 0.11	0.31 ± 0.10	.129
Perimeter (mm)	2.63 ± 0.50	2.42 ± 0.39	.026
Circularity	0.62 ± 0.10	0.65 ± 0.07	.077
VD of SCP (%)
M	4.12 ± 1.48	3.76 ± 1.86	.237
S1	8.96 ± 0.89	9.92 ± 2.42	.030#
S2	9.69 ± 0.84	10.29 ± 2.13	.310#
T1	9.43 ± 1.02	10.11 ± 2.38	.078#
T2	8.92 ± 1.11	9.57 ± 1.88	.077#
I1	8.94 ± 1.29	9.60 ± 2.42	.331#
I2	9.80 ± 0.85	10.14 ± 2.23	.743#
N1	8.22 ± 1.47	9.49 ± 2.61	.006#
N2	10.55 ± 0.83	11.18 ± 2.42	.237#
PD of SCP (%)
M	18.00 ± 7.19	19.53 ± 6.69	.274
S1	46.50 ± 3.80	44.96 ± 4.18	.056
S2	51.19 ± 4.09	52.12 ± 2.98	.150#
T1	47.56 ± 5.97	48.43 ± 5.27	.819#
T2	47.13 ± 5.70	48.29 ± 4.61	.461#
I1	45.04 ± 4.77	45.24 ± 5.63	.967#
I2	50.49 ± 5.43	52.20 ± 3.21	.331#
N1	43.13 ± 4.44	44.55 ± 4.64	.122
N2	52.36 ± 3.77	53.84 ± 2.12	.092#
VD of DCP (%)
M	3.29 ± 1.77	3.04 ± 1.49	.629#
S1	10.80 ± 2.42	10.67 ± 2.42	.801#
S2	8.76 ± 2.31	8.22 ± 2.59	.281#
T1	10.84 ± 2.49	11.04 ± 2.35	.790#
T2	10.18 ± 2.74	10.14 ± 2.89	.925#
I1	9.82 ± 2.49	9.71 ± 2.67	.746#
I2	7.55 ± 2.65	7.33 ± 2.55	.600#
N1	11.10 ± 2.19	11.10 ± 2.39	.994#
N2	9.84 ± 2.39	9.39 ± 2.27	.169#
PD of DCP (%)
M	15.76 ± 9.48	14.75 ± 6.67	.986#
S1	48.47 ± 11.43	47.43 ± 9.78	.481#
S2	38.55 ± 11.12	39.22 ± 9.08	.904#
T1	49.06 ± 12.33	49.82 ± 10.68	.915#
T2	45.22 ± 12.24	46.29 ± 10.89	.775#
I1	43.27 ± 12.42	44.33 ± 11.03	.893#
I2	33.98 ± 11.95	36.12 ± 10.11	.492#
N1	49.55 ± 12.51	50.59 ± 9.81	.964#
N2	44.92 ± 11.77	50.27 ± 6.37	.044#

#At least one group of the parameter did not conform to the normal distribution, and the p-value was obtained by the Mann–Whitney U test.

*Fisher exact test.

VD: vascular density; PD: perfusion density; RPCP: radial peripapillary capillary plexus; SCP: superficial capillary plexus; DCP: deep capillary plexus; FAZ: foveal avascular zone; NDR: diabetic patients without diabetic retinopathy; T: temporal; S: superior; N: nasal; I: inferior; M: middle.

Table 4. Correlation of retinal volume, retinal thickness, and VD and PD of SCP and VD and PD of DCP in the NDR group.

	SPD M	SPD S2	DVD M	DPD M
Retinal volume
Retinal volume S2		0.371**
Retinal volume M	0.415**		0.503**	0.519**
Retinal thickness
Retinal thickness S2		0.549**
Retinal thickness M			0.527**	0.526**

**p < .01.

SPD: perfusion density of superficial capillary plexus; DVD: vessel density of deep capillary plexus; DPD: perfusion density of deep capillary plexus M: middle S: superior.

Yau JWY, Rogers SL, Kawasaki R, Meta-Analysis for Eye Disease (META-EYE) Study Group, et al. Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care. 2012;35(3):556–564.

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Data availability statement

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.