Correlations between Retinal Arterial Morphometric Parameters and Neurodegeneration in Patients with Type 2 Diabetes Mellitus with No or Mild Diabetic Retinopathy
Abstract
:1. Introduction
2. Materials and Methods
2.1. Study Subjects
2.2. SD-OCT Data Acquisition
2.3. Image Analysis Using FWHM Micro-Densitometry Method
2.4. Retinal Artery Morphometry
2.5. Intra-Rater Agreement
2.6. Measurement of Ocular Factors
2.7. Systemic Factors
2.8. Statistical Analysis
3. Results
3.1. Demographic and Clinical Characteristics of the Study Sample
3.2. Morphometry of the Retinal Arteries
3.3. Thickness of the Retinal Layers
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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ICC for RAOD | ICC | 95% CI | ICC for RALD | ICC | 95% CI |
---|---|---|---|---|---|
For single measures | 0.9966 | 0.9958–0.9972 | for single measures | 0.9966 | 0.9959–0.9972 |
For average measures | 0.9983 | 0.9979–0.9986 | for average measures | 0.9983 | 0.9979–0.9986 |
Characteristics | Control | NDR | DR | p-Value |
---|---|---|---|---|
Number of subjects | 32 | 32 | 21 | |
Age, years | 55.34 ± 12.37 (51.054, 59.626) | 60.50 ± 9.95 (57.053, 63.947) | 60.48 ± 9.53 (56.404, 64.556) | 0.112 ^ |
Gender: Male/Female, n | 17/15 | 18/14 | 15/6 | 0.388 # |
BMI, kg/m2 | 27.16 ± 5.03 (25.417, 28.903) | 32.12 ± 7.23 (29.615, 34.625) | 29.44 ± 4.84 (27.369, 31.510) | 0.005 ^ |
Diabetes duration, years | N/A | 9.24 ± 8.10 (6.433, 12.046) | 14.67 ± 6.0 (12.091, 17.249) | 0.006 ˅ |
HbA1c, % | N/A | 9.25 ± 2.30 (8.453, 10.047) | 9.28 ± 1.79 (8.514, 10.046) | 0.397 ˅ |
Blood creatinine, mmol/L | N/A | 0.83 ± 0.21 (0.757, 0.903) | 1.05 ± 0.53 (0.823, 1.277) | 0.849 ˅ |
eGFR, mL/min/1.73 m2 | N/A | 88.19 ± 20.71 (81.014, 95.365) | 74.25 ± 28.61 (62.014, 86.486) | 0.136 ˅ |
Current smoking, n | 8 | 10 | 8 | 0.596 # |
BCVA, logMAR | 0.00 (0) | 0.00 (0.1) | 0.00 (0.1) | 0.185 * |
Treatment with Insulin, n | N/A | 21 | 17 | 0.125 # |
HBP, n | 17 | 24 | 13 | 0.189 # |
Cardiovascular disease, n | 3 | 14 | 12 | <0.001 # |
Dyslipidemia, n | 6 | 18 | 16 | <0.001 # |
Control | NDR | NPDR | p-Value | |
---|---|---|---|---|
RAOD (µm) | 130.71 ± 10.08 (127.217, 134.203) | 133.73 ± 8.44 (130.806, 136.654) | 135.76 ± 10.04 (131.466, 140.054) | 0.155 ^ |
RALD (µm) | 97.21 ± 8.10 (94.404, 100.016) | 98.78 ± 6.87 (96.399, 101.160) | 100.38 ± 8.12 (96.907, 103.853) | 0.338 ^ |
AWT (µm) | 16.75 ± 2.19 (15.991, 17.509) | 17.47 ± 1.90 (16.812, 18.128) | 17.69 ± 2.13 (16.779, 18.601) | 0.211 ^ |
WLR | 0.35 ± 0.05 (0.333, 0.367) | 0.36 ± 0.04 (0.346, 0.374) | 0.35 ± 0.05 (0.329, 0.371) | 0.675 ^ |
WCSA (µm2) | 6065.36 ± 1162.26 (5662.555, 6467.945) | 6391.15 ± 977.05 (6052.626, 6729.674) | 6646.89 ± 1085.16 (6182.768, 7111.012) | 0.151 ^ |
Retinal Layer Thickness (µm) | Control | NDR | NPDR | p-Value | Post-Hoc Analysis with Tukey Test | ||
---|---|---|---|---|---|---|---|
peripapillary RNFL | Control-NDR | Control-NPDR | NDR-NPDR | ||||
Temporal | 71.41 ± 12.90 (66.941, 75.879) | 68.22 ± 12.5 (63.868, 72.572) | 73.29 ± 12.78 (67.952, 78.628) | 0.342 ^ | |||
Temporal-superior | 142.16 ± 20.02 (135.224, 149.096) | 135.63 ± 22.38 (127.876, 143.384) | 138.62 ± 21.28 (129.519, 147.721) | 0.472 ^ | |||
Nasal-superior | 116.38 ± 14.20 (111.46, 121.3) | 115.78 ± 22.32 (108.047, 123.513) | 113.95 ± 23.01 (104.109, 123.791) | 0.907 ^ | |||
Nasal | 78.88 ± 12.97 (74.386, 83.374) | 74.97 ± 13.97 (70.129, 79.810) | 72.76 ± 1322 (67.106, 78.414) | 0.243 ^ | |||
Nasal-inferior | 121.19 ± 21.86 (113.616, 128.764) | 113.88 ± 23.89 (105.603, 122.157) | 105.67 ± 22.22 (96.166, 115.174) | 0.056 ^ | 0.464 | 0.036 | 0.381 |
Temporal-inferior | 144.47 ± 17.36 (108.455, 120.485) | 142.28 ± 20.22 (135.274, 149.286) | 137.05 ± 26.62 (125.665, 148.435) | 0.451 ^ | |||
Average | 103.19 ± 17.47 (97.044, 109.336) | 99.19 ± 10.28 (95.628, 102.752) | 98.48 ± 11.61 (93.514, 103.446) | 0.168 ^ | |||
macular RNFL | |||||||
Central | 12.50 ± 1.97 (11.817, 13.183) | 12.44 ± 2.18 (11.685, 13.195) | 13.57 ± 2.98 (12.295, 14.845) | 0.176 ^ | |||
Center min | 0 (1) | 0 (0) | 0 (2) | 0.224 * | |||
Center max | 23.19 ± 2.63 (22.279, 24.101) | 23.75 ± 3.20 (22.641, 24.859) | 23.81 ± 3.71 (22.926, 25.834) | 0.706 ^ | |||
Inner-temporal | 16.94 ± 1.05 (16.576, 17.304) | 17.59 ± 1.70 (17.001, 18.179) | 18.67 ± 3.02 (17.88, 20.12) | 0.008 ^ | 0.425 | 0.004 | 0.107 |
Inner-nasal | 21.09 ± 1.67 (20.511, 21.669) | 21.66 ± 4.35 (20.153, 23.167) | 22.71 ± 4.44 (21.707, 24.872) | 0.283 ^ | |||
Inner-superior | 24.44 ± 2.80 (21.469, 23.410) | 23.97 ± 3.15 (22.879, 25.061) | 26.29 ± 6.08 (24.602, 29.118) | 0.107 ^ | |||
Inner-inferior | 25.75 ± 2.76 (24.794, 26.706) | 24.56 ± 3.30 (23.417, 25.703) | 26.05 ± 6.26 (21.708, 24.872) | 0.351 ^ | |||
Outer-temporal | 18.59 ± 1.19 (18.178, 19.002) | 19.00 ± 1.48 (18.49, 19.51) | 20.10 ± 3.27 (18.701, 21.499) | 0.029 ^ | 0.733 | 0.018 | 0.112 |
Outer-nasal | 49.19 ± 6.37 (46.983, 51.397) | 45.59 ± 6.49 (43.341, 47.839) | 47.10 ± 11.48 (42.19, 52.01) | 0.201 ^ | |||
Outer-superior | 37.25 ± 5.36 | 35.34 ± 5.31 | 38.19 ± 8.12 | 0.224 ^ | |||
Outer-inferior | 39.22 ± 4.34 (37.716, 40.724) | 38.16 ± 6.25 (35.994, 40.325) | 39.14 ± 9.30 (35.162, 43.118) | 0.781 ^ | |||
Average | 27.22 ± 1.97 (26.537, 27.903) | 26.48 ± 2.58 (25.586, 27.374) | 27.98 ± 5.19 (25.760, 30.199) | 0.259 ^ |
Retinal Layer Thickness (µm) | Control | NDR | NPDR | p-Value * | Post-Hoc Analysis with Tukey Test | ||
GCL | Control-NDR | Control-NPDR | NDR-NPDR | ||||
Central | 16.16 ± 4.68 (14.498, 17.741) | 15.06 ± 4.11 (13.636, 16.484) | 17.81 ± 7.70 (14.517, 21.103) | 0.199 ^ | |||
Center min | 0.5(2) | 1(2) | 0(1.5) | 0.594 * | |||
Center max | 38.81 ± 8.94 (35.712, 41.907) | 36.72 ± 9.74 (33.328, 40.112) | 39.33 ± 9.68 (35.189, 43.470) | 0.544 ^ | |||
Inner-temporal | 47.75 ± 5.44 (45.865, 49.635) | 43.59 ± 6.94 (41.185, 45.994) | 44.67 ± 5.95 (42.125, 47.215) | 0.025 ^ | 0.039 | 0.161 | 0.797 |
Inner-nasal | 52.34 ± 5.56 (50.414, 54.266) | 47.50 ± 6.67 (45.189, 49.811) | 49.86 ± 6.32 (47.157, 52.563) | 0.009 ^ | 0.013 | 0.304 | 0.342 |
Inner-superior | 53.19 ± 4.82 (51.52, 54.86) | 48.47 ± 5.61 (46.526, 50.414) | 50.38 ± 6.11 (47.767, 52.993) | 0.004 ^ | 0.006 | 0.146 | 0.403 |
Inner-inferior | 52.97 ± 4.73 (51.331, 54.609) | 48.47 ± 6.07 (46.367, 50.573) | 48.81 ± 8.98 (44.969, 52.651) | 0.013 ^ | 0.033 | 0.052 | 0.979 |
Outer-temporal | 36.50 ± 3.70 (35.218, 37.782) | 35.22 ± 4.96 (33.501, 36.938) | 35.33 ± 5.58 (32.943, 37.717) | 0.502 ^ | |||
Outer-nasal | 38.53 ± 3.11 (37.452, 39.607) | 37.66 ± 3.53 (36.437, 38.883) | 36.24 ± 4.33 (34.388, 38.092) | 0.082 ^ | |||
Outer-superior | 34.81 ± 3.49 (33.601, 36.019) | 33.72 ± 3.25 (32.594, 34.846) | 33.48 ± 4.32 (31.632, 35.328) | 0.336 ^ | |||
Outer-inferior | 33.56 ± 2.59 (32.663, 34.457) | 32.72 ± 3.59 (31.476, 33.964) | 32.62 ± 3.96 (30.926, 34.314) | 0.500 ^ | |||
Average | 40.65 ± 3.29 (39.510, 41.789) | 38.05 ± 3.95 (36.681, 39.419) | 38.80 ± 4.19 (37.008, 40.592) | 0.023 ^ | 0.031 | 0.229 | 0.626 |
Control | NDR | NPDR | p-Value | Post-Hoc Analysis with Tukey Test | |||
Total retinal thickness | Control-NDR | Control-NPDR | NDR-NPDR | ||||
Central | 280.19 ± 21.38 (272.782, 287.598) | 264.44 ± 22.20 (256.748, 272.132) | 286.19 ± 24.07 (275.895, 296.485) | 0.002 ^ | 0.03 | 0.585 | 0.002 |
Center min | 230.47 ± 19.81 (223.606, 237.334) | 212.97 ± 21.28 (205.597, 220.343) | 230.71 ± 27.96 (218.751,242.668) | 0.003 ^ | 0.015 | 0.999 | 0.013 |
Center max | 326.84 ± 19.81 (319.976, 333.704) | 314.69 ± 22.92 (306.749, 322.631) | 332.43 ± 23.98 (322.174, 342.686) | 0.016 ^ | 0.128 | 0.641 | 0.015 |
Inner-temporal | 332.13 ± 16.38 (326.455, 337.805) | 318.44 ± 18.30 (312.099, 324.780) | 331.71 ± 19.90 (323.199, 340.221) | 0.005 ^ | 0.017 | 0.996 | 0.021 |
Inner-nasal | 348.94 ± 16.24 (343.313, 354.567) | 330.88 ± 21.44 (323.452, 338.308) | 347.43 ± 16.27 (340.471, 354.389) | <0.001 ^ | 0.001 | 0.951 | 0.004 |
Inner-superior | 346.41 ± 16.00 (340.866, 351.954) | 330.75 ± 17.07 (324.836, 336.664) | 342.76 ± 20.31 (334.073, 351.447) | 0.002 ^ | 0.004 | 0.724 | 0.035 |
Inner-inferior | 343.56 ± 15.53 (338.179, 348.941) | 328.53 ± 17.48 (322.474, 334.586) | 339.52 ± 22.04 (330.093, 348.946) | 0.004 ^ | 0.008 | 0.687 | 0.068 |
Outer-temporal | 286.38 ± 10.95 (282.586, 290.174) | 278.41 ± 15.24 (273.129, 283.690) | 287.90 ± 19.08 (279.739, 296.061) | 0.039 ^ | 0.125 | 0.924 | 0.054 |
Outer-nasal | 316.28 ± 13.13 (311.731, 320.829) | 304.66 ± 15.15 (299.411, 309.909) | 314.19 ± 24.17 (303.852, 324.527) | 0.021 ^ | 0.038 | 0.895 | 0.107 |
Outer-superior | 300.66 ± 12.66 (296.274, 305.046) | 288.78 ± 12.15 (284.570, 292.989) | 298.95 ± 20.16 (290.328, 307.572) | 0.004 ^ | 0.010 | 0.904 | 0.033 |
Outer-inferior | 288.38 ± 11.58 (284.368, 292.392) | 280.84 ± 17.60 (274.742, 286.938) | 289.19 ± 17.02 (281.911, 296.469) | 0.081 ^ | |||
Average | 315.88 ± 12.48 (311.556, 320.204) | 302.66 ± 14.07 (297.785, 307.535) | 315.32 ± 16.79 (308.139, 322.501) | <0.001 ^ | 0.003 | 0.988 | 0.004 |
RAOD | RALD | AWT | WLR | WCSA | |
---|---|---|---|---|---|
Univariable Model | Univariable Model | Univariable Model | Univariable Model | Univariable Model | |
Age, years | 0.004 (−0.259, 0.267) (0.976) | −0.065 (−0.278, 0.148) (0.645) | 0.130 (0.074, 0.186) (0.353) | 0.142 (0.140, 0.144) (0.310) | 0.113 (−29.322, 29.548) (0.422) |
Gender, male | 0.061 (−5.141, 5.263) (0.664) | 0.126 (−4.066, 4.318) (0.370) | −0.093 (−1.225, 1.039) (0.506) | −0.197 (−0.221, −0.173) (0.158) | −0.052 (−584.519, 584.416) (0.712) |
Duration of diabetes, years | 0.205 (−0.116, 0.526) (0.141) | 0.134 (−0.131, 0.399) (0.339) | 0.220 (0.150, 0.290) (0.113) | 0.110 (0.108, 0.112) (0.433) | 0.265 (−35.323, 35.853) (0.055) |
HbA1C, % | −0.074 (−1.293, 1.145) (0.602) | −0.139 (−1.117, 0.839) (0.326) | 0.089 (−0.174, 0.352) (0.531) | 0.177 (0.171, 0.183) (0.209) | 0.003 (−136.675, 136.681) (0.981) |
Centralmacular thickness (µm) | 0.270 (0.172, 0.368) (0.051) | 0.228 (0.148, 0.308) (0.100) | 0.194 (0.172, 0.216) (0.163) | 0.041 (0.041, 0.0412) (0.773) | 0.283 (−10.644, 11.210) (0.040) |
Macular thickness average (µm) | 0.126 (−0.029, 0.281) (0.368) | 0.121 (−0.005, 0.247) (0.387) | 0.064 (0.030, 0.098) (0.649) | −0.013 (−0.0128, −0.013) (0.925) | 0.106 (−17.374, 17.586) (0.450) |
Central GCL (µm) | 0.342 (−0.055, 0.739) (0.012) | 0.281 (−0.048, 0.610) (0.041) | 0.260 (0.172, 0.348) (0.060) | 0.074 (0.072, 0.076) (0.597) | 0.353 (−44.112, 44.817) (0.009) |
Average GCL (µm) | 0.228 (−0.388, 0.844) (0.101) | 0.241 (−0.257, 0.739) (0.082) | 0.075 (−0.063, 0.213) (0.594) | −0.082 (−0.086, −0.078) (0.560) | 0.156 (−70.137, 70.449) (0.266) |
Central macular RNFL, (µm) | 0.192 (−0.786, 1.170) (0.168) | 0.177 (−0.618, 0.972) (0.204) | 0.111 (−0.106, 0.328) (0.428) | −0.014 (−0.018, −0.009) (0.920) | 0.181 (−109.760, 110.122) (0.194) |
Average macular RNFL, (µm) | −0.027 (−0.687, 0.633) (0.850) | −0.110 (−0.422, 0.642) (0.432) | 0.144 (0.001, 0.286) (0.304) | 0.194 (0.189, 0.198) (0.164) | −0.015 (−74.209, 74.179) (0.916) |
Average peripapillary RNFL (µm) | 0.183 (−0.050, 0.416) (0.190) | 0.163 (−0.028, 0.354) (0.243) | 0.116 (0.064, 0.168) (0.408) | 0.002 (−0.00001, 0.004) (0.988) | 0.141 (−26.295, 26.577) (0.315) |
RAOD | RALD | AWT | WLR | WCSA | |
---|---|---|---|---|---|
Adjusted Model * | Adjusted Model * | Adjusted Model * | Adjusted Model * | Adjusted Model * | |
Age, years | −0.065 (−0.351, 0.221) (0.666) | −0.119 (−0.348, 0.110) (0.433) | 0.071 (0.011, 0.131) (0.628) | 0.124 (0.122, 0.126) (0.394) | 0.032 (−30.969, 31.033) (0.827) |
Gender, male | −0.014 (−5.458, 5.486) (0.922) | 0.086 (−4.332, 4.504) (0.556) | −0.128 (−1.275, 1.019) (0.369) | −0.207 (−0.231, −0.183) (0.146) | −0.103 (−595.876, 595.669) (0.473) |
Duration of diabetes, years | 0.214 (−0.152, 0.580) (0.170) | 0.111 (−0.185, 0.407) (0.471) | 0.287 (0.210, 0.363) (0.061) | 0.196 (0.194, 0.198) (0.191) | 0.311 (−39.497, 40.119) (0.043) |
HbA1C, % | −0.042 (−1.319, 1.235) (0.775) | −0.134 (−1.166, 0.898) (0.369) | 0.152 (−0.115, 0.419) (0.292) | 0.227 (0.221, 0.233) (0.116) | 0.066 (−138.999, 139.132) (0.648) |
Central macular thickness, µm | −0.263 (0.152, 0.374) (0.078) | 0.193 (0.102, 0.284) (0.199) | 0.248 (0.226, 0.270) (0.088) | 0.120 (0.119, 0.1202) (0.408) | 0.316 (−11.437, 12.069) (0.029) |
Macular thickness average, µm | 0.107 (−0.064, 0.278) (0.469) | 0.070 (−0.069, 0.209) (0.637) | 0.117 (0.081, 0.153) (0.412) | 0.067 (0.0668, 0.0672) (0.636) | 0.136 (−18.399, 18.671) (0.343) |
Central GCL, µm | 0.360 (−0.055, 0.775) (0.011) | 0.283 (−0.061, 0.627) (0.050) | 0.304 (0.215, 0.393) (0.029) | 0.118 (0.116, 0.120) (0.403) | 0.390 (−44.041, 44.821) (0.005) |
Average GCL, µm | 0.273 (−0.442, 0.988) (0.073) | 0.258 (−0.322, 0.838) (0.091) | 0.149 (−0.004, 0.302) (0.319) | −0.043 (−0.047, −0.039) (0.772) | 0.229 (−78.256, 78.714) (0.126) |
Central macular RNFL, µm | 0.180 (−0.882, 1.259) (0.207) | 0.123 (−0.751, 0.997) (0.416) | 0.209 (−0.014, 0.432) (0.150) | 0.113 (0.109, 0.117) (0.434) | 0.247 (−114.687, 115.181) (0.089) |
Average macular RNFL, µm | 0.009 (−0.722, 0.739) (0.952) | −0.129 (−0.715, 0.457) (0.386) | 0.263 (0.116, 0.409) (0.065) | 0.309 (0.305, 0.313) (0.027) | 0.077 (−79.303, 79.457) (0.595) |
Average peripapillary RNFL, µm | 0.247 (−0.011, 0.505) (0.108) | 0.201 (−0.008, 0.410) (0.192) | 0.196 (0.142, 0.250) (0.191) | 0.036 (0.034, 0.038) (0.809) | 0.227 (−27.897, 28.351) (0.130) |
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Damian, I.; Nicoară, S.D. Correlations between Retinal Arterial Morphometric Parameters and Neurodegeneration in Patients with Type 2 Diabetes Mellitus with No or Mild Diabetic Retinopathy. Medicina 2021, 57, 244. https://doi.org/10.3390/medicina57030244
Damian I, Nicoară SD. Correlations between Retinal Arterial Morphometric Parameters and Neurodegeneration in Patients with Type 2 Diabetes Mellitus with No or Mild Diabetic Retinopathy. Medicina. 2021; 57(3):244. https://doi.org/10.3390/medicina57030244
Chicago/Turabian StyleDamian, Ioana, and Simona Delia Nicoară. 2021. "Correlations between Retinal Arterial Morphometric Parameters and Neurodegeneration in Patients with Type 2 Diabetes Mellitus with No or Mild Diabetic Retinopathy" Medicina 57, no. 3: 244. https://doi.org/10.3390/medicina57030244