Journal List > J Korean Ophthalmol Soc > v.58(7) > 1010811

Sang, Joon, Ha, and So: The Changes of Macular Microvasculature and Related Systemic Parameters in Diabetic Patients without Diabetic Retinopathy

Abstract

Purpose

To investigate the systemic parameters related to changes in the retinal microvasculature using optical coherence to-mography angiography (OCTA) in diabetic patients without diabetic retinopathy.

Methods

We retrospectively reviewed the medical records of diabetic patients without diabetic retinopathy. All patients showed normal fundus on dilated fundus examinations. OCTA (DRI OCT Triton, Topcon Corporation, Tokyo, Japan) was performed on a 3 × 3 mm area centered at the fovea. The foveal avascular zone (FAZ) area and vascular density (VD) of the superficial and deep capillary plexus (SCP/DCP) were measured. Multiple regression analysis was conducted to evaluate the relationship be-tween microvascular indexes on OCTA and systemic parameters including sex, age, duration of diabetes mellitus (DM), hemo-globin A1c (HbA1c), total cholesterol, presence of hypertension (HTN) and systolic and diastolic blood pressure (SBP/DBP).

Results

A total of 35 eyes of 35 patients were included in this study. The mean age was 55.7 ± 11.6 years, the mean duration of DM was 52.4 ± 88.7 months and the mean HbA1c was 8.8 ± 2.3%. The FAZ area of the DCP increased significantly as the HbA1c level increased (p < 0.001), but the other parameters, i.e., sex, age, duration of DM, total cholesterol, presence of HTN, SBP and DBP, did not exhibit significant relations in the DCP (p = 0.727, 0.280, 0.385, 0.816, 0.206, 0.055 and 0.092, re-spectively). There were no significant relationships between systemic parameters and the FAZ area in the SCP (p > 0.05). No systemic parameters exhibited significant relationships with VD in either the SCP or the DCP (p > 0.05).

Conclusions

The FAZ area of the DCP detected via OCTA increased as the level of HbA1c increased, although the patients did not show diabetic retinopathy on dilated fundus examinations. Therefore, clinicians should consider this when screening diabetic patients for diabetic retinopathy.

References

1. Koo BK, Moon MK. Are we in the same risk of diabetes mellitus? Gender- and age specific epidemiology of diabetes in 2001 to 2014 in the Korean population. Diabetes Metab J. 2016; 40:175–81.
2. Kahn HA, Hiller R. Blindness caused by diabetic retinopathy. Am J Ophthalmol. 1974; 78:58–67.
crossref
3. Classification of diabetic retinopathy from fluorescein angiograms. ETDRS report number 11. Early Treatment Diabetic Retinopathy Study Research Group. Ophthalmology. 1991; 98((5 Suppl)):807–22.
4. Diabetes Control and Complications Trial Research Group, Nathan DM, Genuth S. . The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med. 1993; 329:977–86.e1.
crossref
5. Lyons TJ, Jenkins AJ, Zheng D. . Diabetic retinopathy and se-rum lipoprotein subclasses in the DCCT/EDIC cohort. Invest Ophthalmol Vis Sci. 2004; 45:910–8.
crossref
6. Klein R, Klein BE, Moss SE. . The Wisconsin epidemiologic study of diabetic retinopathy: III. Prevalence and risk of diabetic retinopathy when age at diagnosis is 30 or more years. Arch Ophthalmol. 1984; 102:527–32.
7. Spaide RF, Klancnik JM Jr, Cooney MJ. Retinal vascular layers imaged by fluorescein angiography and optical coherence tomog-raphy angiography. JAMA Ophthalmol. 2015; 133:45–50.
crossref
8. Jia Y, Tan O, Tokayer J. . Split-spectrum amplitude decorrelation angiography with optical coherence tomography. Opt Express. 2012; 20:4710–25.
9. Al-Sheikh M, Akil H, Pfau M, Sadda SR. Swept-source OCT angiography imaging of the foveal avascular zone and macular capil-lary network density in diabetic retinopathy. Invest Ophthalmol Vis Sci. 2016; 57:3907–13.
crossref
10. de Carlo TE, Chin AT, Bonini Filho MA. . Detection of micro-vascular changes in eyes of patients with diabetes but not clinical diabetic retinopathy using optical coherence tomography angio- graphy. Retina. 2015; 35:2364–70.
11. Di G, Weihong Y, Xiao Z. . A morphological study of the fo-veal avascular zone in patients with diabetes mellitus using optical coherence tomography angiography. Graefes Arch Clin Exp Ophthalmol. 2016; 254:873–9.
crossref
12. Freiberg FJ, Pfau M, Wons J. . Optical coherence tomography angiography of the foveal avascular zone in diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol. 2016; 254:1051–8.
crossref
13. Ji B, Kim HC. Foveal microvascular changes based on optical co-herence tomography angiography in mild nonproliferative diabetic retinopathy. J Korean Ophthalmol Soc. 2016; 57:1723–30.
crossref
14. Coscas F, Glacet-Bernard A, Miere A. . Optical coherence to-mography angiography in retinal vein occlusion: evaluation of su-perficial and deep capillary plexa. Am J Ophthalmol. 2016; 161:160–71.e1-2..
15. Ishibazawa A, Nagaoka T, Takahashi A. . Optical coherence tomography angiography in diabetic retinopathy: a prospective pi-lot study. Am J Ophthalmol. 2015; 160:35–44.e1.
crossref
16. Ting DSW, Tan GSW, Agrawal R. . Optical coherence tomo-graphic angiography in type 2 diabetes and diabetic retinopathy. JAMA Ophthalmol. 2017; 135:306–12.
crossref
17. Dimitrova G, Chihara E, Takahashi H. . Quantitative retinal optical coherence tomography angiography in patients with dia-betes without diabetic retinopathy. Invest Ophthalmol Vis Sci. 2017; 58:190–6.
crossref
18. Durbin MK, An L, Shemonski ND. . Quantification of retinal microvascular density in optical coherence tomographic angiog-raphy images in diabetic retinopathy. JAMA Ophthalmol. 2017; 135:370–6.
crossref

Figure 1.
The optical coherence tomography angiography images of 2 subjects; a 30-year-old female patient with hemoglobin A1c level of 5.9% (A, C, E, G) and a 75-year-old male patient with hemoglobin A1c level of 13.4% (B, D, F, H). Foveal avascular zone area of the superficial (A, B) and deep capillary plexuses (E, F). Converted images of the superficial (C, D) and deep capillary plex-uses (G, H) by adjust threshold tool set to default of Image J to calculate vascular density.
jkos-58-811f1.tif
Table 1.
The demographic and clinical characteristics of the participants
Characteristics Total (n = 35)
Sex, male (n, %) 25 (71.4)
Mean age (years) 55.7 ± 11.6
Mean duration of DM (months) 52.4 ± 88.7
HbA1c (%) 8.8 ± 2.3
Total cholesterol (mg/dL) 188.0 ± 40.1
Presence of HTN (n, %) 10 (28.6)
SBP (mmHg) 119.9 ± 13.6
DBP (mmHg) 76.5 ± 8.8
Superficial FAZ (mm2) 0.35 ± 0.12
Deep FAZ (mm2) 0.59 ± 0.18
Superficial VD (%) 28.97 ± 3.93
Deep VD (%) 32.26 ± 3.54

Values are presented as mean ± SD or n (%) unless otherwise indicated. DM = diabetic mellitus; HbA1c = hemoglobin A1c; HTN = hy-pertension; SBP = systolic blood pressure; DBP = diastolic blood pressure; FAZ = foveal avascular zone; VD = vascular density.

Table 2.
The relationship between the foveal avascular zone area of superficial capillary plexus and systemic parameters
Variables Univariate * Multiple
Coefficient p-value* Coefficient p-value
Sex (female) 0.228 0.188
Age Duration of DM 0.161 -0.143 0.355 0.411
Duration of DM -0.143 0.411
HbA1c 0.189 0.276
Total cholesterol 0.043 0.808
Presence of HTN 0.012 0.944
SBP -0.321 0.060 -0.321 0.060
DBP -0.252 0.145

DM = diabetic mellitus; HbA1c = hemoglobin A1c; HTN = hypertension; SBP = systolic blood pressure; DBP = diastolic blood pressure.

* Univariate linear regression analysis.

Multiple regression analysis with backward elimination.

Table 3.
The relationship between the foveal avascular zone area of deep capillary plexus and systemic parameters
Variables Univariate Multiple
Coefficient p-value* Coefficient p-value
Sex (female) 0.061 0.727
Age 0.188 0.280
Duration of DM -0.152 0.385
HbA1c 0.652 <0.001 0.652 <0.001
Total cholesterol -0.041 0.816
Presence of HTN -0.219 0.206
SBP -0.327 0.055 -0.165 0.234
DBP -0.289 0.092 -0.122 0.381

DM = diabetic mellitus; HbA1c = hemoglobin A1c; HTN = hypertension; SBP = systolic blood pressure; DBP = diastolic blood pressure.

* Univariate linear regression analysis.

Multiple regression analysis with backward elimination.

Table 4.
The relationship between the vascular density of superficial capillary plexus and systemic parameters
Variables Univariate Multiple
Coefficient p-value* Coefficient p-value
Sex (female) 0.154 0.378
Age -0.289 0.092 -0.215 0.213
Duration of DM -0.329 0.054 -0.329 0.054
HbA1c -0.046 0.792
Total cholesterol -0.099 0.573
Presence of HTN -0.086 0.623
SBP -0.058 0.741
DBP 0.162 0.352

DM = diabetic mellitus; HbA1c = hemoglobin A1c; HTN = hypertension; SBP = systolic blood pressure; DBP = diastolic blood pressure

* Univariate linear regression analysis.

Multiple regression analysis with backward elimination.

Table 5.
The relationship between the vascular density of deep capillary plexus and systemic parameters
Variables Univariate Multiple
Coefficient p-value* Coefficient p-value
Sex (female) -0.029 0.869
Age -0.234 0.176
Duration of DM -0.298 0.082 -0.298 0.082
HbA1c 0.001 0.995
Total cholesterol -0.180 0.300
Presence of HTN -0.278 0.106
SBP -0.108 0.536
DBP -0.062 0.722

DM = diabetic mellitus; HbA1c = hemoglobin A1c; HTN = hypertension; SBP = systolic blood pressure; DBP = diastolic blood pressure.

* Univariate linear regression analysis.

Multiple regression analysis with backward elimination.

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