Skip to main content

Advertisement

Log in

Foveal vasculature changes and nonperfusion in patients with diabetes types I and II with no evidence of diabetic retinopathy

  • Retinal Disorders
  • Published:
Graefe's Archive for Clinical and Experimental Ophthalmology Aims and scope Submit manuscript

Abstract

Purpose

To analyze the foveal avascular zone (FAZ) in patients with diabetes and no retinopathy vs. controls using OCT angiography (OCT-A).

Methods

Prospective, observational clinical study. Type I and II diabetics with no retinopathy and healthy control patients underwent OCT-A. The FAZ size and capillary density were calculated using Image J and Adobe Photoshop CS8. Statistical analysis was performed using one-way ANOVA with Tukey’s multiple comparison test and the Pearson correlation test.

Results

Fifty-two eyes of 28 diabetic patients and 28 eyes of 16 healthy controls were enrolled. Type I diabetes patients had a longer disease duration than type II (30.3 ± 10.3 vs. 12.3 ± 9.7 years). The mean superficial capillary plexus (SCP) of the FAZ area was 0.27 ± 0.1, 0.36 ± 0.14, and 0.27 ± 0.12 mm2, for the type I, type II, and controls (p = 0.0058) and was significantly larger in type II diabetics (p < 0.05). The mean DCP (deep capillary plexus) FAZ was significantly larger in type II diabetics vs. controls (0.67 ± 0.2 and 0.52 ± 0.16 mm2 respectively) (p < 0.05). Both type I and type II SCP capillary density were significantly lower than the controls (p < 0.05, p < 0.005), and DCP capillary density was significantly lower in type II vs. controls (p < 0.005).

Conclusions

Type I patients showed fewer changes in the FAZ than the type II group, although their duration of diabetes was longer. Larger studies are needed to better analyze the differences between type I and type II diabetics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Cheung N, Mitchell P, Wong TY (2010) Diabetic retinopathy. Lancet 376:124–136

    Article  Google Scholar 

  2. Antonetti DA, Klein R, Gardner TW (2012) Diabetic retinopathy. N Engl J Med 366:1227–1239

    Article  CAS  Google Scholar 

  3. Varma R, Bressler NM, Doan QV et al (2014) Prevalence of and risk factors for diabetic macular edema in the United States. JAMA Ophthalmol 132:1334–1340

    Article  Google Scholar 

  4. Spaide RF, Fujimoto JG, Waheed NK, Sadda SR, Staurenghi G (2018) Optical coherence tomography angiography. Prog Retin Eye 64:1–55

    Article  Google Scholar 

  5. Coscas G, Lupidi M, Coscas F, Chhablani J, Cagini C (2018) Optical coherence tomography angiography in healthy subjects and diabetic patients. Ophthalmologica 239:61–73

    Article  Google Scholar 

  6. Yannuzzi LA, Rohrer KT, Tindel LJ et al (1986) Fluorescein angiography complication survey. Ophthalmology 93:611–617

    Article  CAS  Google Scholar 

  7. Mendis KR, Balaratnasingam C, Yu P et al (2010) Correlation of histologic and clinical images to determine the diagnostic value of fluorescein angiography for studying capillary detail. Invest Ophthalmol Vis Sci 51:5864–5869

    Article  Google Scholar 

  8. Spaide RF, Klancnik JM Jr, Cooney MJ (2015) Retinal vascular layers imaged by fluorescein angiography and optical coherence tomography angiography. JAMA Ophthalmol 133:45–50

    Article  Google Scholar 

  9. De Carlo TE, Chin AT, Bonini Filho MA et al (2015) Detection of microvascular changes in eyes of patients with diabetes but not clinical diabetic retinopathy using optical coherence tomography angiography. Retina 35:2364–2370

    Article  Google Scholar 

  10. Dimitrova G, Chihara H, Takahashi H, Amano H, Okazaki K (2017) Quantitative retinal optical coherence tomography angiography in patients with diabetes without diabetic retinopathy quantitative retinal OCTA in diabetes without DR investigative. Ophthalmol Vis Sci 58:190–196

    Article  Google Scholar 

  11. Carnevali A, Sacconi R, Corbelli E et al (2017) Optical coherence tomography angiography analysis of retinal vascular plexuses and choriocapillaris in patients with type 1 diabetes without diabetic retinopathy. Acta Diabetol 54:695–702

    Article  CAS  Google Scholar 

  12. Simonett JM, Scarinci F, Picconi F et al (2017) Early microvascular retinal changes in optical coherence tomography angiography in patients with type 1 diabetes mellitus. Acta Ophthalmol 95:751–755

    Article  Google Scholar 

  13. Gołębiewska J, Olechowski A, Wysocka-Mincewicz M et al (2017) Optical coherence tomography angiography vessel density in children with type 1 diabetes. PLoS One 12:e0186479

    Article  Google Scholar 

  14. Kim K, Kim ES, Yu SY (2018) Optical coherence tomography angiography analysis of foveal microvascular changes and inner retinal layer thinning in patients with diabetes. Br J Ophthalmol 102:1226–1231

    Article  Google Scholar 

  15. Klein R, Klein BE, Moss SE, Davis MD, DeMets DL (1984) The Wisconsin epidemiological study of diabetic retinopathy II. Prevalence and risk of diabetic retinopathy when age at diagnosis is less than 30 years. Arch Ophthalmol 102:520–526

    Article  CAS  Google Scholar 

  16. Shields CL, Say EA, Samara WA, Khoo CT, Mashayekhi A, Shields JA (2016) Optical coherence tomography angiography of the macula after plaque radiotherapy of choroidal melanoma: comparison of irradiated versus nonirradiated eyes in 65 patients. Retina 36:1493–1505

    Article  Google Scholar 

  17. Romero-Aroca P, Navarro-Gil R, Valls-Mateu A et al (2017) Differences in incidence of diabetic retinopathy between type 1 and 2 diabetes mellitus: a nine-year follow-up study. Br J Ophthalmol 101:1346–1351

    Article  Google Scholar 

  18. Looker HC, Nyangoma SO, Cromie DT et al (2014) Scottish diabetes research network epidemiology group; Scottish diabetic retinopathy collaborative. Rates of referable eye disease in the Scottish national diabetic retinopathy screening programme. Br J Ophthalmol 98:790–795

    Article  CAS  Google Scholar 

  19. Klein R, Knudtson MD, Lee KE, Gangnon R, Klein BE (2008) The Wisconsin epidemiologic study of diabetic retinopathy: XXII the twenty-five-year progression of retinopathy in persons with type 1 diabetes. Ophthalmology 115:1859–1868

    Article  Google Scholar 

  20. Agemy SA, Scripsema NK, Shah CM et al (2015) Retinal vascular perfusion density mapping using optical coherence tomography angiography in normals and diabetic retinopathy patients. Retina. 35:2353–2363

    Article  Google Scholar 

  21. Hwang TS, Gao SS, Liu L et al (2016) Automated quantification of capillary nonperfusion using optical coherence tomography angiography in diabetic retinopathy. JAMA Ophthalmol 134:367–373

    Article  Google Scholar 

  22. Di G, Weihong Y, Xiao Z et al (2016) Morphological study of the foveal avascular zone in patients with diabetes mellitus using optical coherence tomography angiography. Graefes Arch Clin Exp Ophthalmol 254:873–879

    Article  Google Scholar 

  23. Kim DY, Fingler J, Zawadzki RJ et al (2012) Noninvasive imaging of the foveal avascular zone with high-speed, phase-variance optical coherence tomography. Invest Ophthalmol Vis Sci 53:85–92

    Article  Google Scholar 

  24. Schwartz DM, Fingler J, Kim DY et al (2014) Phase-variance optical coherence tomography: a technique for noninvasive angiography. Ophthalmology 121:180–187

    Article  Google Scholar 

  25. Takase N, Nozaki M, Kato A et al (2015) Enlargement of foveal avascular zone in diabetic eyes evaluated by en face optical coherence tomography angiography. Retina 35:2377–2383

    Article  Google Scholar 

  26. Bhanushali D, Anegondi N, Gadde SG et al (2016) Linking retinal microvasculature features with severity of diabetic retinopathy using optical coherence tomography angiography. Invest Ophthalmol Vis Sci 57:519–525

    Article  Google Scholar 

  27. Lachin JM, Genuth S, Cleary P, Davis MD, Nathan DM (2000) Diabetes control and complications trial/epidemiology of diabetes interventions and complications research group. Retinopathy and nephropathy in patients with type 1 diabetes four years after a trial of intensive therapy. N Engl J Med 342:381–389

    Article  Google Scholar 

  28. White NH, Sun W, Cleary PA et al (2010) DCCT-EDIC research group. Effect of prior intensive therapy in type 1 diabetes on 10-year progression of retinopathy in the DCCT/EDIC: comparison of adults and adolescents. Diabetes 59:1244–1253

    Article  CAS  Google Scholar 

  29. Lachin JM, White NH, Hainsworth DP et al (2015) Diabetes control and complications trial (DCCT)/epidemiology of diabetes interventions and complications (EDIC) research group. Effect of intensive diabetes therapy on the progression of diabetic retinopathy in patients with type 1 diabetes: 18 years of follow-up in the Dcct/edic. Diabetes 64:631–642

    Article  CAS  Google Scholar 

  30. Styles CJ, Dodds W, Watkins P, McHugh D, Blach R (2000) Development of proliferative retinopathy in patients with long-standing insulin-dependent diabetes mellitus. Eye (Lond) 14:851–854

    Article  CAS  Google Scholar 

Download references

Funding

The study was financially supported by an unrestricted grant from Research to Prevent Blindness.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Charles C. Barr.

Ethics declarations

Conflict of interest

The authors have no conflict of interest or financial interest to disclose.

Ethical approval

All procedures performed in this study were in accordance with the ethical standards of the University of Louisville IRB. Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fleissig, E., Adhi, M., Sigford, D.K. et al. Foveal vasculature changes and nonperfusion in patients with diabetes types I and II with no evidence of diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol 258, 551–556 (2020). https://doi.org/10.1007/s00417-019-04588-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00417-019-04588-5

Keywords

Navigation