Skip to main content

Advertisement

Log in

Optical coherence tomography angiography analysis of the choriocapillary layer in treatment-naïve diabetic eyes

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

Abstract

Purpose

To evaluate the capillary flow density (CFD) of choriocapillary (CC) microvasculature using optical coherence tomography angiography (OCT-A) in diabetic eyes and the association of CFD and systemic and metabolic factors.

Methods

Cross-sectional study. This study enrolled 282 eyes of 146 subjects, including 43 healthy control eyes, 56 diabetic eyes without diabetic retinopathy (DR), 43 eyes with mild nonproliferative DR (NPDR), 54 eyes with moderate NPDR, 38 eyes with severe NPDR, and 48 eyes with proliferative DR (PDR). CFD was measured in the CC layer. Clinical data were collected. Multiple linear regression analyses were performed to identify associated clinical variables.

Results

CFD in the CC layer presented a downward trend with DR progression. Comparisons of CFD in the CC layer between adjacent stages of DR revealed significant differences between severe NPDR and PDR using both 3-mm and 6-mm scan patterns (P = 0.003, P = 0.001). CFD in the CC layer in DR with diabetic macular edema (DME) was less than that in DR without DME using both 3-mm and 6-mm scan patterns (P < 0.001, P < 0.001). Coronary artery disease and atherosclerosis in other locations, estimated glomerular filtration rate, and increased HbA1c were associated with CFD in the CC layer using both 3-mm and 6-mm scan patterns (all P values < 0.05).

Conclusions

OCT-A revealed decreased CFD in the CC layer in the PDR stage and the presence of DME. Diabetic patients with apparently decreased CFD should be assessed carefully under general conditions.

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

Similar content being viewed by others

References

  1. Yau JW, Rogers SL, Kawasaki R, Lamoureux EL, Kowalski JW, Bek T, Chen SJ, Dekker JM, Fletcher A, Grauslund J, Haffner S, Hamman RF, Ikram MK, Kayama T, Klein BE, Klein R, Krishnaiah S, Mayurasakorn K, O'Hare JP, Orchard TJ, Porta M, Rema M, Roy MS, Sharma T, Shaw J, Taylor H, Tielsch JM, Varma R, Wang JJ, Wang N, West S, Xu L, Yasuda M, Zhang X, Mitchell P, Wong TY (2012) Global prevalence and major risk factors of diabetic retinopathy. Diabetes Care 35:556–564. https://doi.org/10.2337/dc11-1909

    Article  PubMed  PubMed Central  Google Scholar 

  2. Antonetti DA, Klein R, Gardner TW (2012) Diabetic retinopathy. N Engl J Med 366:1227–1239. https://doi.org/10.1056/NEJMra1005073

    Article  CAS  PubMed  Google Scholar 

  3. Hayreh SS (2001) Blood flow in the optic nerve head and factors that may influence it. Prog Retin Eye Res 20:595–624

    Article  CAS  PubMed  Google Scholar 

  4. McLeod DS, Lutty GA (1994) High-resolution histologic analysis of the human choroidal vasculature. Invest Ophthalmol Vis Sci 35:3799–3811

    CAS  PubMed  Google Scholar 

  5. Lutty GA (2013) Effects of diabetes on the eye. Invest Ophthalmol Vis Sci 54:Orsf81–Orsf87. https://doi.org/10.1167/iovs.13-12979

    Article  PubMed  PubMed Central  Google Scholar 

  6. Takahashi A, Nagaoka T, Sato E, Yoshida A (2008) Effect of panretinal photocoagulation on choroidal circulation in the foveal region in patients with severe diabetic retinopathy. Br J Ophthalmol 92:1369–1373. https://doi.org/10.1136/bjo.2007.136028

    Article  CAS  PubMed  Google Scholar 

  7. Agrawal R, Xin W, Keane PA, Chhablani J, Agarwal A (2016) Optical coherence tomography angiography: a non-invasive tool to image end-arterial system. Expert Rev Med Devices 13:519–521. https://doi.org/10.1080/17434440.2016.1186540

    Article  CAS  PubMed  Google Scholar 

  8. Jia Y, Bailey ST, Wilson DJ, Tan O, Klein ML, Flaxel CJ, Potsaid B, Liu JJ, Lu CD, Kraus MF, Fujimoto JG, Huang D (2014) Quantitative optical coherence tomography angiography of choroidal neovascularization in age-related macular degeneration. Ophthalmology 121:1435–1444. https://doi.org/10.1016/j.ophtha.2014.01.034

    Article  PubMed  Google Scholar 

  9. Choi W, Waheed NK, Moult EM, Adhi M, Lee B, De Carlo T, Jayaraman V, Baumal CR, Duker JS, Fujimoto JG (2017) Ultrahigh speed swept source optical coherence tomography angiography of retinal and choriocapillaris alterations in diabetic patients with and without retinopathy. Retina (Philadelphia, Pa) 37:11–21. https://doi.org/10.1097/iae.0000000000001250

    Article  CAS  Google Scholar 

  10. Conti FF, Qin VL, Rodrigues EB, Sharma S, Rachitskaya AV, Ehlers JP, Singh RP (2018) Choriocapillaris and retinal vascular plexus density of diabetic eyes using split-spectrum amplitude decorrelation spectral-domain optical coherence tomography angiography. Br J Ophthalmol 103:452–456. https://doi.org/10.1136/bjophthalmol-2018-311903

  11. Nesper PL, Roberts PK, Onishi AC, Chai H, Liu L, Jampol LM, Fawzi AA (2017) Quantifying microvascular abnormalities with increasing severity of diabetic retinopathy using optical coherence tomography angiography. Invest Ophthalmol Vis Sci 58:Bio307–bio315. https://doi.org/10.1167/iovs.17-21787

    Article  PubMed  PubMed Central  Google Scholar 

  12. Carnevali A, Sacconi R, Corbelli E, Tomasso L, Querques L, Zerbini G, Scorcia V, Bandello F, Querques G (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 

  13. Lim HB, Kim YW, Kim JM, Jo YJ, Kim JY (2018) The importance of signal strength in quantitative assessment of retinal vessel density using optical coherence tomography angiography. Sci Rep 8:12897. https://doi.org/10.1038/s41598-018-31321-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Levey AS, Stevens LA, Schmid CH, Zhang YL, Castro AF 3rd, Feldman HI, Kusek JW, Eggers P, Van Lente F, Greene T, Coresh J (2009) A new equation to estimate glomerular filtration rate. Ann Intern Med 150:604–612

    Article  PubMed  PubMed Central  Google Scholar 

  15. Zhang M, Hwang TS, Campbell JP, Bailey ST, Wilson DJ, Huang D, Jia Y (2016) Projection-resolved optical coherence tomographic angiography. Biomed Opt Express 7:816–828. https://doi.org/10.1364/boe.7.000816

    Article  PubMed  PubMed Central  Google Scholar 

  16. Fukushima I, McLeod DS, Lutty GA (1997) Intrachoroidal microvascular abnormality: a previously unrecognized form of choroidal neovascularization. Am J Ophthalmol 124:473–487

    Article  CAS  PubMed  Google Scholar 

  17. Funatsu H, Yamashita H, Ikeda T, Nakanishi Y, Kitano S, Hori S (2002) Angiotensin II and vascular endothelial growth factor in the vitreous fluid of patients with diabetic macular edema and other retinal disorders. Am J Ophthalmol 133:537–543

    Article  CAS  PubMed  Google Scholar 

  18. Melancia D, Vicente A, Cunha JP, Abegao Pinto L, Ferreira J (2016) Diabetic choroidopathy: a review of the current literature. Graefes Arch Clin Exp Ophthalmol 254:1453–1461. https://doi.org/10.1007/s00417-016-3360-8

    Article  PubMed  Google Scholar 

  19. Paine SK, Mondal LK, Borah PK, Bhattacharya CK, Mahanta J (2017) Pro- and antiangiogenic VEGF and its receptor status for the severity of diabetic retinopathy. Mol Vis 23:356–363

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Ting DSW, Tan GSW, Agrawal R, Yanagi Y, Sie NM, Wong CW, San Yeo IY, Lee SY, Cheung CMG, Wong TY (2017) Optical coherence tomographic angiography in type 2 diabetes and diabetic retinopathy. JAMA Ophthalmol 135:306–312. https://doi.org/10.1001/jamaophthalmol.2016.5877

    Article  PubMed  Google Scholar 

  21. Lee DH, Yi HC, Bae SH, Cho JH, Choi SW, Kim H (2018) Risk factors for retinal microvascular impairment in type 2 diabetic patients without diabetic retinopathy. PLoS One 13:e0202103. https://doi.org/10.1371/journal.pone.0202103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Van Belle E, Rivard A, Chen D, Silver M, Bunting S, Ferrara N, Symes JF, Bauters C, Isner JM (1997) Hypercholesterolemia attenuates angiogenesis but does not preclude augmentation by angiogenic cytokines. Circulation 96:2667–2674

    Article  PubMed  Google Scholar 

  23. Pedersen BK (2017) Anti-inflammatory effects of exercise: role in diabetes and cardiovascular disease. Eur J Clin Investig 47:600–611. https://doi.org/10.1111/eci.12781

    Article  CAS  Google Scholar 

  24. Ohno T, Takamoto S, Motomura N (2008) Diabetic retinopathy and coronary artery disease from the cardiac surgeon’s perspective. Ann Thorac Surg 85:681–689. https://doi.org/10.1016/j.athoracsur.2007.07.066

    Article  PubMed  Google Scholar 

  25. Pant S, Deshmukh A, Gurumurthy GS, Pothineni NV, Watts TE, Romeo F, Mehta JL (2014) Inflammation and atherosclerosis--revisited. J Cardiovasc Pharmacol Ther 19:170–178. https://doi.org/10.1177/1074248413504994

    Article  CAS  PubMed  Google Scholar 

  26. Hsieh YT, Tsai MJ, Tu ST, Hsieh MC (2018) Association of abnormal renal profiles and proliferative diabetic retinopathy and diabetic macular edema in an Asian population with type 2 diabetes. JAMA Ophthalmol 136:68–74. https://doi.org/10.1001/jamaophthalmol.2017.5202

    Article  PubMed  Google Scholar 

  27. Chang YC, Wu WC (2013) Dyslipidemia and diabetic retinopathy. Rev Diabet Stud 10:121–132. https://doi.org/10.1900/rds.2013.10.121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Sas KM, Kayampilly P, Byun J, Nair V, Hinder LM, Hur J, Zhang H, Lin C, Qi NR, Michailidis G, Groop PH, Nelson RG, Darshi M, Sharma K, Schelling JR, Sedor JR, Pop-Busui R, Weinberg JM, Soleimanpour SA, Abcouwer SF, Gardner TW, Burant CF, Feldman EL, Kretzler M, Brosius FC 3rd, Pennathur S (2016) Tissue-specific metabolic reprogramming drives nutrient flux in diabetic complications. JCI Insight 1:e86976. https://doi.org/10.1172/jci.insight.86976

    Article  PubMed  PubMed Central  Google Scholar 

  29. Suzuma I, Hata Y, Clermont A, Pokras F, Rook SL, Suzuma K, Feener EP, Aiello LP (2001) Cyclic stretch and hypertension induce retinal expression of vascular endothelial growth factor and vascular endothelial growth factor receptor-2: potential mechanisms for exacerbation of diabetic retinopathy by hypertension. Diabetes 50:444–454

    Article  CAS  PubMed  Google Scholar 

  30. Sizmaz S, Kucukerdonmez C, Pinarci EY, Karalezli A, Canan H, Yilmaz G (2013) The effect of smoking on choroidal thickness measured by optical coherence tomography. Br J Ophthalmol 97:601–604. https://doi.org/10.1136/bjophthalmol-2012-302393

    Article  PubMed  Google Scholar 

  31. Teberik K (2019) The effect of smoking on macular, choroidal, and retina nerve fiber layer thickness. Turk J Ophthalmol 49:20–24. https://doi.org/10.4274/tjo.galenos.2018.80588

    Article  PubMed  PubMed Central  Google Scholar 

  32. Remen T, Pintos J, Abrahamowicz M, Siemiatycki J (2018) Risk of lung cancer in relation to various metrics of smoking history: a case-control study in Montreal. BMC Cancer 18:1275. https://doi.org/10.1186/s12885-018-5144-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

Thanks are due to Chenxi Zhang, Minghang Pei, and Shan Wu for collecting data and supporting this study.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Youxin Chen.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. 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. 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

Yang, J., Wang, E., Zhao, X. et al. Optical coherence tomography angiography analysis of the choriocapillary layer in treatment-naïve diabetic eyes. Graefes Arch Clin Exp Ophthalmol 257, 1393–1399 (2019). https://doi.org/10.1007/s00417-019-04326-x

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00417-019-04326-x

Keywords

Navigation