Skip to main content

Advertisement

Log in

Quantitative analysis of early retinal vascular changes in type 2 diabetic patients without clinical retinopathy by optical coherence tomography angiography

  • Original Paper
  • Published:
International Ophthalmology Aims and scope Submit manuscript

Abstract

Purpose

To investigate the quantitative differences in optical coherence tomography angiography (OCTA) data between type 2 diabetes patients without clinically detectable diabetic retinopathy (DR) and healthy subjects.

Methods

Thirty-nine patients with type 2 diabetes without DR and 41 age- and sex-matched healthy controls were recruited. The vessel density and foveal avascular zone (FAZ) area in the superficial capillary plexus and deep capillary plexus were measured using Nidek RS-3000 Advance® and compared between patient cohorts. Foveal vessel density (%) and FAZ (%) were also calculated.

Results

A significant decrease in vessel density has been observed in the deep capillary plexus of the patients compared to healthy individuals (5.58 ± 0.98 mm2 versus 6.15 ± 0.89 mm2, p < 0.001). However, there were no significant differences in other parameters between cohorts (p > 0.05 in all parameters). Despite the decrease of deep capillary plexus density in the macular region, there was no significant change observed in foveal vessel density (p:0.44). It has also been observed that the duration of diabetes mellitus correlates with vessel density decrease in deep capillary plexus (R:–0.52; p < 0.001). In both groups, all parameters in deep capillary plexus were significantly higher than superficial capillary plexus (p < 0.001 for all parameters).

Conclusions

OCTA can identify quantitative changes in DCP before the manifestation of clinically apparent retinopathy. DCP-VD reduction may be an earlier finding than FAZ enlargement. Despite the reduction of VD, FVD could be preserved for a certain period of time in DM patients.

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

Availability of data and material

Data and material are available.

References

  1. Flaxman SR, Bourne RRA, Resnikoff S et al (2017) Global causes of blindness and distance vision impairment 1990–2020: a systematic review and meta-analysis. Lancet Glob Heal 5:1221–1234. https://doi.org/10.1016/S2214-109X(17)30393-5

    Article  Google Scholar 

  2. Williams R, Airey M, Baxter H et al (2004) Epidemiology of diabetic retinopathy and macular oedema: a systematic review. Eye 18:963–983. https://doi.org/10.1038/sj.eye.6701476

    Article  CAS  PubMed  Google Scholar 

  3. Antonetti DA, Barber AJ, Bronson SK et al (2006) Diabetic retinopathy: seeing beyond glucose-induced microvascular disease. Diabetes 55:2401–2411. https://doi.org/10.2337/db05-1635

    Article  CAS  PubMed  Google Scholar 

  4. Lecleire-Collet A, Tessier LH, Massin P et al (2005) Advanced glycation end products can induce glial reaction and neuronal degeneration in retinal explants. Br J Ophthalmol 89:1631–1633. https://doi.org/10.1136/bjo.2005.079491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Spaide R, Fujimoto J, Waheed N et al (2017) Optical coherence tomography angiography. Prog Retin Eye Res 101:985–988. https://doi.org/10.1136/bjophthalmol-2016-309200

    Article  Google Scholar 

  6. Corvi F, Pellegrini M, Erba S et al (2018) Reproducibility of vessel density, fractal dimension, and foveal avascular zone using 7 different optical coherence tomography angiography devices. Am J Ophthalmol 186:25–31. https://doi.org/10.1016/j.ajo.2017.11.011

    Article  PubMed  Google Scholar 

  7. Al-Sheikh M, Tepelus TC, Nazikyan T, Sadda SR (2017) Repeatability of automated vessel density measurements using optical coherence tomography angiography. Br J Ophthalmol 101:449–452. https://doi.org/10.1136/bjophthalmol-2016-308764

    Article  PubMed  Google Scholar 

  8. Battista M, Borrelli E, Sacconi R et al (2020) Optical coherence tomography angiography in diabetes: a review. Eur J Ophthalmol 30:411–416. https://doi.org/10.1177/1120672119899901

    Article  PubMed  Google Scholar 

  9. Olafsdottir E, Andersson DKG, Dedorsson I et al (2016) Early detection of type 2 diabetes mellitus and screening for retinopathy are associated with reduced prevalence and severity of retinopathy. Acta Ophthalmol 94:232–239. https://doi.org/10.1111/aos.12954

    Article  PubMed  Google Scholar 

  10. Li Z, Wen X, Zeng P et al (2019) Do microvascular changes occur preceding neural impairment in early-stage diabetic retinopathy? Evidence based on the optic nerve head using optical coherence tomography angiography. Acta Diabetol 56:531–539. https://doi.org/10.1007/s00592-019-01288-8

    Article  PubMed  Google Scholar 

  11. Zeng Y, Cao D, Yu H et al (2019) Early retinal neurovascular impairment in patients with diabetes without clinically detectable retinopathy. Br J Ophthalmol 103:1747–1752. https://doi.org/10.1136/bjophthalmol-2018-313582

    Article  PubMed  Google Scholar 

  12. Cao D, Yang D, Huang Z et al (2018) Optical coherence tomography angiography discerns preclinical diabetic retinopathy in eyes of patients with type 2 diabetes without clinical diabetic retinopathy. Acta Diabetol 55:469–477. https://doi.org/10.1007/s00592-018-1115-1

    Article  PubMed  Google Scholar 

  13. Dimitrova G, Chihara E, Takahashi H et al (2017) Quantitative retinal optical coherence tomography angiography in patients with diabetes without diabetic retinopathy. Investig Ophthalmol Vis Sci 58:190–196. https://doi.org/10.1167/iovs.16-20531

    Article  Google Scholar 

  14. Vujosevic S, Muraca A, Alkabes M et al (2019) Early microvascular and neural changes in patients with type 1 and type 2 diabetes mellitus without clinical signs of diabetic retinopathy. Retina 39:435–445. https://doi.org/10.1097/IAE.0000000000001990

    Article  PubMed  Google Scholar 

  15. Choi W, Waheed NK, Moult EM et al (2017) Ultrahigh speed oct angiography of retinal and choriocapillaris alterations in diabetic patients with and without retinopathy using swept source optical coherence tomography. Retina 37:11–21. https://doi.org/10.1007/s11897-014-0247-z.Pathophysiology

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Spaide RF, Curcio CA (2017) Evaluation of segmentation of the superficial and deep vascular layers of the retina by optical coherence tomography angiography instruments in normal eyes. JAMA Ophthalmol 135:259–262. https://doi.org/10.1001/jamaophthalmol.2016.5327

    Article  PubMed  Google Scholar 

  17. Coscas F, Sellam A, Glacet-Bernard A et al (2016) Normative data for vascular density in superficial and deep capillary plexuses of healthy adults assessed by optical coherence tomography angiography. Investig Ophthalmol Vis Sci 57:OCT211-OCT223. Doi: https://doi.org/10.1167/iovs.15-18793

  18. Hussain N, Hussain A (2016) Diametric measurement of foveal avascular zone in healthy young adults using optical coherence tomography angiography. Int J Retin Vitr 2:27. https://doi.org/10.1186/s40942-016-0053-8

    Article  Google Scholar 

  19. Lupidi M, Coscas F, Cagini C et al (2016) Automated quantitative analysis of retinal microvasculature in normal eyes on optical coherence tomography angiography. Am J Ophthalmol 169:9–23. https://doi.org/10.1016/j.ajo.2016.06.008

    Article  PubMed  Google Scholar 

  20. Niestrata-Ortiz M, Fichna P, Stankiewicz W, Stopa M (2019) Enlargement of the foveal avascular zone detected by optical coherence tomography angiography in diabetic children without diabetic retinopathy. Graefe’s Arch Clin Exp Ophthalmol 257:689–697. https://doi.org/10.1007/s00417-019-04264-8

    Article  CAS  Google Scholar 

  21. Fernández-Vigo JI, Kudsieh B, Shi H et al (2020) Normative database and determinants of macular vessel density measured by optical coherence tomography angiography. Clin Exp Ophthalmol 48:44–52. https://doi.org/10.1111/ceo.13648

    Article  PubMed  Google Scholar 

  22. Oh J, Baik DJ, Ahn J (2020) Inter-relationship between retinal and choroidal vasculatures using optical coherence tomography angiography in normal eyes. Eur J Ophthalmol 30:48–57. https://doi.org/10.1177/1120672118816225

    Article  PubMed  Google Scholar 

  23. Scarinci F, Picconi F, Giorno P et al (2018) Deep capillary plexus impairment in patients with type 1 diabetes mellitus with no signs of diabetic retinopathy revealed using optical coherence tomography angiography. Acta Ophthalmol 96:264–265. https://doi.org/10.1111/aos.13510

    Article  Google Scholar 

  24. 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. https://doi.org/10.1007/s00592-017-0996-8

    Article  CAS  PubMed  Google Scholar 

  25. Simó R, Stitt AW, Gardner TW (2018) Neurodegeneration in diabetic retinopathy: Does it really matter? Diabetologia 61:1902–1912. https://doi.org/10.1007/s00125-018-4692-1

    Article  PubMed  PubMed Central  Google Scholar 

  26. Dimitrova G, Chihara E (2019) Implication of deep-vascular-layer alteration detected by optical coherence tomography angiography for the pathogenesis of diabetic retinopathy. Ophthalmologica 241:179–182. https://doi.org/10.1159/000495624

    Article  PubMed  Google Scholar 

  27. Cybulska-Heinrich AK, Baertschi M, Loesche CC et al (2015) Patients with diabetic retinopathy have high retinal venous pressure. EPMA J 6:5. https://doi.org/10.1186/s13167-015-0027-1

    Article  PubMed  PubMed Central  Google Scholar 

  28. Suzuki N, Hirano Y, Tomiyasu T et al (2016) Retinal hemodynamics seen on optical coherence tomography angiography before and after treatment of retinal vein occlusion. Investig Opthalmology Vis Sci 57:5681. https://doi.org/10.1167/iovs-16-20648

    Article  Google Scholar 

  29. Bek T (2000) Histopathology and pathophysiology of diabetic retinopathy. In: van Bijsterveld O (ed) Diabetic retinopathy. Martin Dunitz, London, pp 169–189

    Google Scholar 

  30. Nesper PL, Roberts PK, Onishi AC, et al (2017) Quantifying microvascular abnormalities with ıncreasing severity of diabetic retinopathy using optical coherence tomography angiography. Investig Opthalmology Vis Sci 58:BIO307. Doi: https://doi.org/10.1167/iovs.17-21787

  31. Sambhav K, Abu-Amero KK, Chalam KV (2017) deep capillary macular perfusion indices obtained with OCT angiography correlate with degree of nonproliferative diabetic retinopathy. Eur J Ophthalmol 27:716–729. https://doi.org/10.5301/ejo.5000948

    Article  PubMed  Google Scholar 

  32. Hasegawa N, Nozaki M, Takase N et al (2016) new insights into microaneurysms in the deep capillary plexus detected by optical coherence tomography angiography in diabetic macular edema. Invest Ophthalmol Vis Sci 57:348. https://doi.org/10.1167/iovs.15-18782

    Article  Google Scholar 

  33. Dupas B, Minvielle W, Bonnin S et al (2018) Association between vessel density and visual acuity in patients with diabetic retinopathy and poorly controlled type 1 diabetes. JAMA Ophthalmol 136:721–728. https://doi.org/10.1001/jamaophthalmol.2018.1319

    Article  PubMed  PubMed Central  Google Scholar 

  34. 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. https://doi.org/10.1371/journal.pone.0186479

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Li T, Jia Y, Wang S et al (2019) Retinal microvascular abnormalities in children with type 1 diabetes mellitus without visual impairment or diabetic retinopathy. Invest Ophthalmol Vis Sci 60:990. https://doi.org/10.1167/iovs.18-25499

    Article  PubMed  Google Scholar 

  36. 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. https://doi.org/10.1097/IAE.0000000000000882

    Article  PubMed  Google Scholar 

  37. Forte R, Haulani H, Jürgens I (2018) Quantitative and qualitative analysis of the three capillary plexuses and choriocapillaris in patients with type 1 and type 2 diabetes mellitus without clinical signs of diabetic retinopathy. Retina 1:333–344. https://doi.org/10.1097/iae.0000000000002376

    Article  Google Scholar 

  38. Shiihara H, Sakamoto T, Yamashita T et al (2017) Reproducibility and differences in area of foveal avascular zone measured by three different optical coherence tomographic angiography instruments. Sci Rep 7:9853. https://doi.org/10.1038/s41598-017-09255-5

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Muhammed Altinisik.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of Manisa Celal Bayar University (Date: 02.05.2018 / No:20.478.486).

Informed consent

Informed consent was obtained from all individual participants included in the study.

Consent to participate

Informed consents were obtained from the patients.

Consent for publication

Patients signed informed consent regarding publishing their data.

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

Altinisik, M., Kahraman, N.S., Kurt, E. et al. Quantitative analysis of early retinal vascular changes in type 2 diabetic patients without clinical retinopathy by optical coherence tomography angiography. Int Ophthalmol 42, 367–375 (2022). https://doi.org/10.1007/s10792-022-02230-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10792-022-02230-8

Keywords

Navigation