Retinal Microvascular Changes in Association with Endothelial Glycocalyx Damage and Arterial Stiffness in Patients with Diabetes Mellitus Type 2: A Cross-Sectional Study in a Greek Population
Abstract
:1. Introduction
2. Methods
Statistical Analysis
3. Results
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
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Age (years, mean ± SD) | 66.6 ± 8.7 |
Gender (n, %) Male Female | 38 (58.5%) 27 (41.5%) |
Smoking (n, %) | 22 (33.8%) |
DM duration (years, mean ± SD) | 16.4 ± 11.2 |
HbA1c (%, mean ± SD) | 7.2 ± 1.1 |
Total cholesterol (mg/dL, mean ± SD) | 187.3 ± 42.9 |
LDL (mg/dL, mean ± SD) | 113.5 ± 31.4 |
HDL (mg/dL, mean ± SD) | 43.8 ± 14.2 |
Triglycerides (mg/dL, mean ± SD) | 152.4 ± 63.8 |
Hypertension (n, %) | 48 (73.8%) |
Dyslipidemia (n, %) | 52 (80.0%) |
Neuropathy (n, %) | 15 (23.1%) |
Nephropathy (n, %) | 6 (9.2%) |
Diabetic macular edema (n, %) | 28 (43.1%) |
Diabetic retinopathy (n, %) No Mild non-proliferative Moderate non-proliferative Severe non-proliferative Proliferative | 20 (30.8%) 3 (4.6%) 14 (21.5%) 23 (35.4%) 5 (7.7%) |
Visual acuity (decimal, mean ± SD) | 0.44 ± 0.19 |
Intraocular pressure (mmHg, mean ± SD) | 13.4 ± 3.1 |
Lens status (n, %) Phakic Pseudophakic | 42 (64.6%) 23 (35.4%) |
Glycocalyx PBR (mean ± SD) | |
5–25 μm | 2.20 ± 0.26 |
5–9 μm | 1.28 ± 0.23 |
10–19 μm | 2.33 ± 0.28 |
20–25 μm | 2.74 ± 0.43 |
Vessel wall compliance | |
cSBP (mean ± SD, mmHg) | 130.4 ± 20.6 |
cDBP (mean ± SD, mmHg) | 77.6 ± 10.1 |
PP (mean ± SD, mmHg) | 50.7 ± 26.4 |
Aix (mean ± SD, %) | 16.3 ± 23.6 |
PWV (mean ± SD, m/s) | 13.5 ± 4.9 |
Macular Thickness (μm) | |
Central subfield thickness (mean ± SD) | 257.4 ± 36.2 |
Parafoveal superior (mean ± SD) | 278.5 ± 31.3 |
Parafoveal inferior (mean ± SD) | 273.0 ± 29.9 |
Parafoveal nasal (mean ± SD) | 290.5 ± 31.8 |
Parafoveal temporal (mean ± SD) | 280.6 ± 46.2 |
Perifoveal superior (mean ± SD) | 316.7 ± 34.7 |
Perifoveal inferior (mean ± SD) | 316.9 ± 34.2 |
Perifoveal nasal (mean ± SD) | 313.3 ± 31.6 |
Perifoveal temporal (mean ± SD) | 318.4 ± 43.6 |
RNFL thickness (μm) | |
Average (mean ± SD) | 100.1 ± 12.9 |
Superior (mean ± SD) | 120.2 ± 23.4 |
Inferior (mean ± SD) | 125.6 ± 18.0 |
Nasal (mean ± SD) | 75.9 ± 14.4 |
Temporal (mean ± SD) | 78.8 ± 17.3 |
Macular OCT-A | |
VD, Central (%, mean ± SD) | 18.9 ± 5.5 |
VD, Superior (%, mean ± SD) | 41.2 ± 4.73 |
VD, Inferior (%, mean ± SD) | 40.8 ± 4.6 |
VD, Nasal (%, mean ± SD) | 41.5 ± 5.4 |
VD, Temporal (%, mean ± SD) | 42.3 ± 4.6 |
FAZ area (mm2, mean ± SD) | 0.343± 0.146 |
FAZ perimeter (mm, mean ± SD) | 2.723 ± 0.569 |
FAZ circularity index (mean ± SD) | 0.560 ± 0.079 |
Peripapillary OCT-A | |
VD, Average (%, mean ± SD) | 41.5 ± 3.19 |
VD, Superior (%, mean ± SD) | 46.9 ± 4.6 |
VD, Inferior (%, mean ± SD) | 47.9 ± 4.35 |
VD, Nasal (%, mean ± SD) | 40.9 ± 5.31 |
VD, Temporal (%, mean ± SD) | 44.2 ± 3.79 |
Eye Imaging (Dependent Variables) | Univariate OR (95% CI) | p-Value | Multivariate OR (95% CI), Adjusting for Gender, Age *, DM Duration * | p-Value |
---|---|---|---|---|
Diabetic Retinopathy (Yes vs. No) | 1.53 (0.53–4.41) | 0.433 | 2.06 (0.63–6.67) | 0.230 |
Diabetic Macular Edema (Yes vs. No) | 1.38 (0.52–3.69) | 0.515 | 1.33 (0.49–3.62) | 0.575 |
OCT parameters | ||||
Central Subfield Thickness (≥271 μm vs. <271 μm) | 1.54 (0.58–4.09) | 0.389 | 1.43 (0.53–3.91) | 0.481 |
Perifoveal Superior Thickness (≥318 μm vs. <318 μm) | 1.52 (0.57–4.06) | 0.400 | 1.80 (0.64–5.03) | 0.265 |
Perifoveal Inferior Thickness (≥314 μm vs. <314 μm) | 1.18 (0.44–3.14) | 0.746 | 1.30 (0.47–3.56) | 0.616 |
Perifoveal Nasal Thickness (≥319 μm vs. <319 μm) | 1.20 (0.45–3.18) | 0.714 | 1.33 (0.49–3.63) | 0.579 |
Perifoveal Temporal Thickness (≥322 μm vs. <322 μm) | 1.98 (0.74–5.31) | 0.176 | 2.17 (0.76–6.18) | 0.145 |
Parafoveal Superior Thickness (≥269 μm vs. <269 μm) | 1.05 (0.40–2.79) | 0.915 | 1.16 (0.42–3.16) | 0.778 |
Parafoveal Inferior Thickness (≥266 μm vs. <266 μm) | 1.54 (0.58–4.09) | 0.389 | 1.55 (0.57–4.26) | 0.391 |
Parafoveal Nasal Thickness (≥283 μm vs. <283 μm) | 1.54 (0.58–4.09) | 0.389 | 1.53 (0.63–4.76) | 0.290 |
Parafoveal Temporal Thickness (≥265 μm vs. <265 μm) | 1.20 (0.45–3.18) | 0.714 | 1.24 (0.46–3.35) | 0.677 |
Macular OCT-A parameters | ||||
FAZ area (≥0.304 mm2 vs. <0.304 mm2) | 1.66 (0.62–4.46) | 0.318 | 1.62 (0.59–4.43) | 0.344 |
FAZ perimeter (≥2.601 mm vs. <2.601 mm) | 1.00 (0.37–2.67) | > 0.999 | 1.04 (0.38–2.84) | 0.943 |
FAZ circularity (≥0.568 vs. <0.568) | 1.29 (0.48–3.44) | 0.617 | 1.15 (0.40–3.31) | 0.799 |
Vessel Density Central (≥19.82% vs. <19.82%) | 0.60 (0.22–1.62) | 0.318 | 0.59 (0.21–1.62) | 0.303 |
Vessel Density Superior (≥41.38% vs. <41.38%) | 1.00 (0.37–2.67) | > 0.999 | 1.06 (0.39–2.91) | 0.905 |
Vessel Density Inferior (≥41.05% vs. <41.05%) | 1.29 (0.48–3.44) | 0.617 | 1.20 (0.40–3.61) | 0.741 |
Vessel Density Nasal (≥42.19% vs. <42.19%) | 0.78 (0.29–2.08) | 0.617 | 0.76 (0.27–2.09) | 0.590 |
Vessel Density Temporal (≥41.98% vs. <41.98%) | 0.78 (0.29–2.08) | 0.617 | 0.78 (0.28–2.18) | 0.644 |
OCT optic nerve parameters | ||||
RNFL Average Thickness (≥101 μm vs. <101 μm) | 1.20 (0.45–3.18) | 0.714 | 1.19 (0.44–3.25) | 0.734 |
RNFL Superior Thickness (≥124 μm vs. <124 μm) | 1.20 (0.45–3.18) | 0.714 | 1.28 (0.47–3.48) | 0.631 |
RNFL Inferior Thickness (≥126 μm vs. <126 μm) | 0.73 (0.28–1.94) | 0.531 | 0.79 (0.29–2.15) | 0.640 |
RNFL Nasal Thickness (≥73 μm vs. <73 μm) | 1.54 (0.58–4.09) | 0.389 | 1.62 (0.58–4.53) | 0.354 |
RNFL Temporal Thickness (≥77 μm vs. <77 μm) | 2.56 (0.94–6.96) | 0.066 | 2.61 (0.92–7.40) | 0.071 |
OCT-A optic nerve parameters | ||||
Vessel Density Superior (≥47.74% vs. <47.74%) | 0.34 (0.12–0.93) | 0.037 | 0.37 (0.12–1.12) | 0.079 |
Vessel Density Inferior (≥48.17% vs. <48.17%) | 0.57 (0.21–1.52) | 0.263 | 0.52 (0.19–1.48) | 0.223 |
Vessel Density Nasal (≥40.9% vs. <40.9%) | 0.94 (0.35–2.48) | 0.897 | 0.99 (0.36–2.68) | 0.997 |
Vessel Density Temporal (≥43.9% vs. <43.9%) | 0.44 (0.16–1.20) | 0.108 | 0.47 (0.16–1.35) | 0.161 |
Eye Imaging (Dependent Variables) | Univariate OR (95% CI) | p-Value | Multivariate OR (95% CI), Adjusting for Gender, Age *, DM Duration * | p-Value |
---|---|---|---|---|
Diabetic Retinopathy (Yes vs. No) | 2.79 (0.93–8.33) | 0.067 | 3.10 (0.94–10.18) | 0.063 |
Diabetic Macular Edema (Yes vs. No) | 1.78 (0.66–4.78) | 0.252 | 1.74 (0.64–4.70) | 0.277 |
OCT parameters | ||||
Central Subfield Thickness (≥271 μm vs. <271 μm) | 0.94 (0.35–2.48) | 0.897 | 0.89 (0.33–2.41) | 0.824 |
Perifoveal Superior Thickness (≥318 μm vs. <318 μm) | 1.96 (0.73–5.28) | 0.182 | 2.01 (0.73–5.54) | 0.179 |
Perifoveal Inferior Thickness (≥314 μm vs. <314 μm) | 0.71 (0.26–1.91) | 0.498 | 0.72 (0.26–1.94) | 0.511 |
Perifoveal Nasal Thickness (≥319 μm vs. <319 μm) | 0.44 (0.16–1.20) | 0.108 | 0.43 (0.16–1.18) | 0.100 |
Perifoveal Temporal Thickness (≥322 μm vs. <322 μm) | 1.20 (0.45–3.18) | 0.714 | 1.14 (0.42–3.11) | 0.804 |
Parafoveal Superior Thickness (≥269 μm vs. <269 μm) | 0.82 (0.31–2.19) | 0.697 | 0.82 (0.31–2.22) | 0.701 |
Parafoveal Inferior Thickness (≥266 μm vs. <266 μm) | 0.57 (0.21–1.52) | 0.263 | 0.54 (0.20–1.49) | 0.235 |
Parafoveal Nasal Thickness (≥283 μm vs. <283 μm) | 0.73 (0.28–1.94) | 0.531 | 0.73 (0.27–1.96) | 0.533 |
Parafoveal Temporal Thickness (≥265 μm vs. <265 μm) | 0.94 (0.35–2.48) | 0.897 | 0.92 (0.35–2.47) | 0.875 |
Macular OCT-A parameters | ||||
FAZ area (≥0.304 mm2 vs. <0.304 mm2) | 2.79 (1.01–7.70) | 0.048 | 2.88 (1.03–8.04) | 0.044 |
FAZ perimeter (≥2.601 mm vs. <2.601 mm) | 2.79 (1.01–7.70) | 0.048 | 2.82 (1.01–7.89) | 0.048 |
FAZ circularity (≥0.568 vs. <0.568) | 1.00 (0.37–2.67) | > 0.999 | 1.04 (0.36–2.96) | 0.947 |
Vessel Density Central (≥19.82% vs. <19.82%) | 0.47 (0.17–1.27) | 0.135 | 0.47 (0.17–1.29) | 0.143 |
Vessel Density Superior (≥41.38% vs. <41.38%) | 0.78 (0.29–2.08) | 0.617 | 0.79 (0.29–2.14) | 0.639 |
Vessel Density Inferior (≥41.05% vs. <41.05%) | 1.00 (0.37–2.67) | >0.999 | 1.07 (0.36–3.16) | 0.909 |
Vessel Density Nasal (≥42.19% vs. <42.19%) | 0.36 (0.13–0.99) | 0.048 | 0.36 (0.13–1.02) | 0.054 |
Vessel Density Temporal (≥41.98% vs. <41.98%) | 0.47 (0.17–1.27) | 0.135 | 0.46 (0.16–1.30) | 0.143 |
OCT optic nerve parameters | ||||
RNFL Average Thickness (≥101 μm vs. <101 μm) | 0.73 (0.28–1.94) | 0.531 | 0.77 (0.28–2.07) | 0.598 |
RNFL Superior Thickness (≥124 μm vs. <124 μm) | 1.20 (0.45–3.18) | 0.714 | 1.26 (0.47–3.40) | 0.643 |
RNFL Inferior Thickness (≥126 μm vs. <126 μm) | 0.57 (0.21–1.52) | 0.263 | 0.59 (0.22–1.62) | 0.307 |
RNFL Nasal Thickness (≥73 μm vs. <73 μm) | 1.54 (0.58–4.09) | 0.389 | 1.69 (0.61–4.67) | 0.312 |
RNFL Temporal Thickness (≥77 μm vs. <77 μm) | 0.73 (0.28–1.94) | 0.531 | 0.69 (0.25–1.89) | 0.473 |
OCT-A optic nerve parameters | ||||
Vessel Density Superior (≥47.74% vs. <47.74%) | 0.94 (0.35–2.48) | 0.897 | 1.03 (0.35–3.01) | 0.963 |
Vessel Density Inferior (≥48.17% vs. <48.17%) | 0.73 (0.28–1.94) | 0.531 | 0.75 (0.28–2.06) | 0.579 |
Vessel Density Nasal (≥40.9% vs. <40.9%) | 1.20 (0.45–3.18) | 0.714 | 1.26 (0.47–3.40) | 0.643 |
Vessel Density Temporal (≥43.9% vs. <43.9%) | 1.54 (0.58–4.09) | 0.389 | 1.54 (0.55–4.36) | 0.413 |
Eye Imaging (Dependent Variables) | Univariate OR (95% CI) | p-Value | Multivariate OR (95% CI), Adjusting for Gender, Age *, DM Duration * | p-Value |
---|---|---|---|---|
Diabetic Retinopathy (Yes vs. No) | 1.80 (0.62–5.27) | 0.283 | 3.43 (0.92–12.83) | 0.067 |
Diabetic Macular Edema (Yes vs. No) | 2.45 (0.89–6.74) | 0.081 | 3.05 (1.00–9.34) | 0.050 |
OCT parameters | ||||
Central Subfield Thickness (≥271 μm vs. <271 μm) | 2.14 (0.79–5.79) | 0.136 | 2.54 (0.84–7.65) | 0.099 |
Perifoveal Superior Thickness (≥318 μm vs. <318 μm) | 2.14 (0.79–5.82) | 0.135 | 3.37 (1.07–10.60) | 0.038 |
Perifoveal Inferior Thickness (≥314 μm vs. <314 μm) | 1.91 (0.70–5.22) | 0.208 | 2.47 (0.81–7.54) | 0.111 |
Perifoveal Nasal Thickness (≥319 μm vs. <319 μm) | 0.78 (0.29–2.08) | 0.617 | 0.88 (0.31–2.53) | 0.819 |
Perifoveal Temporal Thickness (≥322 μm vs. <322 μm) | 2.14 (0.79–5.79) | 0.136 | 3.37 (1.04–10.90) | 0.043 |
Parafoveal Superior Thickness (≥269 μm vs. <269 μm) | 2.44 (0.89–6.65) | 0.082 | 3.47 (1.11–10.78) | 0.032 |
Parafoveal Inferior Thickness (≥266 μm vs. <266 μm) | 1.65 (0.62–4.44) | 0.319 | 1.78 (0.61–5.24) | 0.294 |
Parafoveal Nasal Thickness (≥283 μm vs. <283 μm) | 1.00 (0.38–2.66) | >0.999 | 1.15 (0.40–3.30) | 0.790 |
Parafoveal Temporal Thickness (≥265 μm vs. <265 μm) | 2.78 (1.01–7.64) | 0.048 | 3.41 (1.11–10.49) | 0.032 |
Macular OCT-A parameters | ||||
FAZ area (≥0.304 mm2 vs. <0.304 mm2) | 0.64 (0.24–1.73) | 0.380 | 0.55 (0.19–1.63) | 0.283 |
FAZ perimeter (≥2.601 mm vs. <2.601 mm) | 0.56 (0.21–1.52) | 0.258 | 0.64 (0.22–1.86) | 0.408 |
FAZ circularity (≥0.568 vs. <0.568) | 1.38 (0.52–3.71) | 0.528 | 1.28 (0.42–3.92) | 0.670 |
Vessel Density Central (≥19.82% vs. <19.82%) | 2.02 (0.74–5.52) | 0.168 | 1.90 (0.65–5.54) | 0.239 |
Vessel Density Superior (≥41.38% vs. <41.38%) | 1.38 (0.51–3.71) | 0.528 | 1.49 (0.51–4.35) | 0.467 |
Vessel Density Inferior (≥41.05% vs. <41.05%) | 1.78 (0.66–4.83) | 0.258 | 1.88 (0.57–6.18) | 0.297 |
Vessel Density Nasal (≥42.19% vs. <42.19%) | 0.83 (0.31–2.22) | 0.707 | 0.62 (0.21–1.86) | 0.393 |
Vessel Density Temporal (≥41.98% vs. <41.98%) | 0.83 (0.31–2.22) | 0.707 | 0.75 (0.25–2.25) | 0.612 |
OCT optic nerve parameters | ||||
RNFL Average Thickness (≥101 μm vs. <101 μm) | 1.28 (0.48–3.43) | 0.617 | 1.03 (0.36–2.98) | 0.950 |
RNFL Superior Thickness (≥124 μm vs. <124 μm) | 0.60 (0.23–1.62) | 0.319 | 0.51 (0.17–1.50) | 0.221 |
RNFL Inferior Thickness (≥126 μm vs. <126 μm) | 0.69 (0.26–1.84) | 0.454 | 0.58 (0.19–1.72) | 0.324 |
RNFL Nasal Thickness (≥73 μm vs. <73 μm) | 1.65 (0.62–4.44) | 0.319 | 1.54 (0.53–4.51) | 0.431 |
RNFL Temporal Thickness (≥77 μm vs. <77 μm) | 1.28 (0.48–3.43) | 0.617 | 1.29 (0.44–3.78) | 0.648 |
OCT-A optic nerve parameters | ||||
Vessel Density Superior (≥47.74% vs. <47.74%) | 0.47 (0.17–1.27) | 0.136 | 0.43 (0.13–1.40) | 0.161 |
Vessel Density Inferior (≥48.17% vs. <48.17%) | 1.28 (0.48–3.43) | 0.617 | 1.19 (0.40–3.47) | 0.757 |
Vessel Density Nasal (≥40.9% vs. <40.9%) | 1.88 (0.70–5.07) | 0.213 | 1.96 (0.67–5.73) | 0.219 |
Vessel Density Temporal (≥43.9% vs. <43.9%) | 0.60 (0.23–1.62) | 0.319 | 0.90 (0.30–2.64) | 0.843 |
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Agapitou, C.; Sergentanis, T.N.; Thymis, J.; Pavlidis, G.; Lampsas, S.; Korakas, E.; Kountouri, A.; Pliouta, L.; Karmiris, E.; Lagiou, A.; et al. Retinal Microvascular Changes in Association with Endothelial Glycocalyx Damage and Arterial Stiffness in Patients with Diabetes Mellitus Type 2: A Cross-Sectional Study in a Greek Population. J. Pers. Med. 2024, 14, 995. https://doi.org/10.3390/jpm14090995
Agapitou C, Sergentanis TN, Thymis J, Pavlidis G, Lampsas S, Korakas E, Kountouri A, Pliouta L, Karmiris E, Lagiou A, et al. Retinal Microvascular Changes in Association with Endothelial Glycocalyx Damage and Arterial Stiffness in Patients with Diabetes Mellitus Type 2: A Cross-Sectional Study in a Greek Population. Journal of Personalized Medicine. 2024; 14(9):995. https://doi.org/10.3390/jpm14090995
Chicago/Turabian StyleAgapitou, Chrysa, Theodoros N. Sergentanis, John Thymis, George Pavlidis, Stamatios Lampsas, Emmanouil Korakas, Aikaterini Kountouri, Loukia Pliouta, Efthymios Karmiris, Areti Lagiou, and et al. 2024. "Retinal Microvascular Changes in Association with Endothelial Glycocalyx Damage and Arterial Stiffness in Patients with Diabetes Mellitus Type 2: A Cross-Sectional Study in a Greek Population" Journal of Personalized Medicine 14, no. 9: 995. https://doi.org/10.3390/jpm14090995