J Korean Ophthalmol Soc.  2017 Jul;58(7):811-817. 10.3341/jkos.2017.58.7.811.

The Changes of Macular Microvasculature and Related Systemic Parameters in Diabetic Patients without Diabetic Retinopathy

• Choi SW
• Cho JH
• Kim HK
• Bae SH

• KMID: 2387155
• DOI: http://doi.org/10.3341/jkos.2017.58.7.811

Abstract

PURPOSE
To investigate the systemic parameters related to changes in the retinal microvasculature using optical coherence tomography 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 between microvascular indexes on OCTA and systemic parameters including sex, age, duration of diabetes mellitus (DM), hemoglobin 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, respectively). 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.

Keyword

Diabetic mellitus; Foveal avascular zone; Optical coherence tomography angiography; Vascular density

MeSH Terms

Angiography
Blood Pressure
Capillaries
Cholesterol
Diabetes Mellitus
Diabetic Retinopathy*
Humans
Hypertension
Mass Screening
Medical Records
Microvessels*
Neptune
Retinaldehyde
Retrospective Studies
Tomography, Optical Coherence
Cholesterol
Retinaldehyde

Figure

• 

  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.

Reference

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.

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.