Optical coherence tomography-angiography in diabetic retinopathy diagnosis and monitoring

Cover Page


Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription or Fee Access

Abstract

Optical coherence tomography-angiography is a modern noninvasive method of 3D imaging and quantitative analysis of the retinal and choroidal microvasculature. It allows detecting manifestation and progression of diabetic retinopathy, planning treatment and evaluating its results.Optical coherence tomography angiography expands our understanding of microvascular changes in retinal vascular plexuses at different disease stages and deepens the understanding of its pathogenesis.

Full Text

Restricted Access

About the authors

Natalia V. Pomytkina

S.N. Fyodorov Eye Microsurgery Federal State Institution

Author for correspondence.
Email: dvk@khvmntk.ru
ORCID iD: 0000-0003-3757-8351
SPIN-code: 4862-2111
Scopus Author ID: 56880370100
ResearcherId: AAI-3050-2020

Cand. Sci. (Med.), Ophthalmologist of Highest Qualification of Laser Surgery Department

Russian Federation, 211, Tikhookeanskaya str., Khabarovsk, 680033

Evgenii L. Sorokin

S.N. Fyodorov Eye Microsurgery Federal State Institution; Far-Eastern State Medical University

Email: dvk@khvmntk.ru
ORCID iD: 0000-0002-2028-1140
SPIN-code: 4516-1429
Scopus Author ID: 7006545279
ResearcherId: AAI-2986-2020

Doctor of Medical Science, Professor, Deputy Head for Scientific Work, Ophthalmologist of Highest Qualification, Professor of the General and Clinical Surgery Department

Russian Federation, 211, Tikhookeanskaya str., Khabarovsk, 680033; 35, Karl Marx str., Khabarovsk, 680000

References

  1. Hwang TS, Jia Y, Gao SS, et al. Optical coherence tomography angiography features of diabetic retinopathy. Retina. 2015;35(11): 2371–2376. doi: 10.1097/IAE.0000000000000716
  2. Ishibazawa A, Nagaoka T, Takahashi A, et al. Optical coherence tomography angiography in diabetic retinopathy: a prospective pilot study. Am J Ophthalmol. 2015;160(1):35–44. doi: 10.1016/j.ajo.2015.04.021
  3. de Carlo TE, Chin AT, Bonini Filho MA, et al. Detection of microvascular changes in eyes of patients with diabetes but not clinical diabetic retinopathy using optical coherence tomography angiography. Retina. 2015;35(11):2364–2370. doi: 10.1097/IAE.0000000000000882
  4. Jia Y, Tan O, Tokayer J, et al. Split-spectrum amplitude-decorrelation angiography with optical coherence tomography. Opt Express. 2012;20(4):4710–4725. doi: 10.1364/OE.20.004710
  5. Mastropasqua R, Di Antonio L, Di Staso S, et al. Optical coherence tomography angiography in retinal vascular diseases and choroidal neovascularization. J Ophthalmol. 2015;2015:343515. doi: 10.1155/2015/343515
  6. Lumbroso B, Huang D, Chen CJ, et al. Clinical OCT Angiography Atlas. Moscow; 2017. (In Russ.)
  7. Geitzenauer W, Hitzenberger C, Schmidt-Erfurth UM. Retinal optical coherence tomography: past, present and future perspectives. Br J Ophthalmol. 2011;95(2):171–177. doi: 10.1136/bjo.2010.182170
  8. Leitgeb R, Schmetterer L, Drexler W, et al. Real-time assessment of retinal blood flow with ultrafast acquisition by color Doppler Fourier domain optical coherence tomography. Opt. Express. 2003;11(23):3116–3121. doi: 10.1364/oe.11.003116
  9. Wang Y, Bower BA, Izatt JA, et al. In vivo total retinal blood flow measurement by Fourier domain Doppler optical coherence tomography. J Biomed Opt. 2007;12(4):041215. doi: 10.1117/1.2772871
  10. Ruminski D, Bukowska D, Gorczynska I, et al. Angiogram visualization and total velocity blood flow assessment based on intensity information analysis of OCT data. Proceedings Volume 8213, Optical Coherence Tomography and Coherence Domain Optical Methods in Biomedicine XVI; 821306 (2012). San Francisco, California, United States. doi: 10.1117/12.911573
  11. Gill A, Cole ED, Novais EA, et al. Visualization of changes in the foveal avascular zone in both observed and treated diabeticmacular edema using optical coherence tomography angiography. Int J Retina Vitreous. 2017;3:19. doi: 10.1186/s40942-017-0074-y
  12. Wang Q, Chan S, Yang JY, et al. Vascular density in retina and choriocapillaris as measured by optical coherence tomography angiography. Am J Ophthalmol. 2016;168:95–109. doi: 10.1016/j.ajo.2016.05.005
  13. Zhang A, Zhang Q, Chen CL, Wang RK. Methods and algorithms for optical coherence tomography-based angiography: a review and comparison. J Biomed Opt. 2015;20(10):100901. doi: 10.1117/1.JBO.20.10.100901
  14. Kurysheva NI, Maslova EV. Optical coherence tomography angiography in glaucoma diagnosis. Vestnik oftalmologii. 2016;132(5): 98–102. (In Russ.) doi: 10.17116/oftalma2016132598-102
  15. Neroev VV, Okhotsimskaya TD, Fadeeva VA. An account of retinal microvascular changes in diabetes acquired by OCT angiography. Russian Ophthalmological Journal. 2017;10(2):40–45. (In Russ.) doi: 10.21516/2072-0076-2017-10-2-40-45
  16. Ioyleva EE, Krivosheeva MS, Andrusyakova EP. OCT-angiography parameters of the macular area of the retina and optic nerve in healthy young people. Rossiyskaya detskaya oftal’mologiya. 2019;(3):38–42. (In Russ.) doi: 10.25276/2307-6658-2019-3-38-42
  17. Mariampillai A, Leung M K, Jarvi M, et al. Optimized speckle variance OCT imaging of microvasculature. Opt Lett. 2010;35(8):1257–1259. doi: 10.1364/OL.35.001257
  18. Maslova EV. Issledovaniye roli i mesta OKT-angiografii v diagnostike glaukomy [dissertation]. Moscow; 2016. (In Russ.)
  19. Savastano MC, Lumbroso B, Rispoli M. In vivo characterization of retinal vascularization morphology using optical coherence tomography angiography. Retina. 2015;35(11):2196–2203. doi: 10.1097/IAE.0000000000000635
  20. Spaide RF, Klancnik JM, Cooney MJ. Retinal vascular layers imaged by fluorescein angiography and optical coherence tomography angiography. JAMA Ophthalmol. 2015;133(1):45–50. doi: 10.1001/jamaophthalmol.2014.3616
  21. Tultseva SN, Astakhov YS, Rukhovets AG, Titarenko AI. Diagnostic value of OCT-angiography and regional hemodynamic assessmentin patients with retinal vein occlusion. Ophthalmology Journal. 2017;10(2):40–48. (In Russ.) doi: 10.17816/OV10240-48
  22. Freiberg FJ, Pfau M, Wons J, et al. Optical coherence tomography angiography of the foveal avascular zone in diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol. 2016;254(6):1051–1058. doi: 10.1007/s00417-015-3148-2
  23. Budzinskaya MV, Shelankova AV, Mikhaylova MA, et al. Analysis of changes in central macular thickness based on optical coherence tomography angiography findings in retinal vein occlusion. Vestnik oftalmologii. 2016;132(5):15–22. (In Russ.) doi: 10.17116/oftalma2016132515-22
  24. Park JJ, Soetikno BT, Fawzi AA. Characterization of the middle capillary plexus using optical coherence tomography angiography in healthy and diabetic eyes. Retina. 2016;36(11):2039–2050. doi: 10.1097/IAE.0000000000001077
  25. Alexandrov AA, Aznabaev BM, Mukhamadeev TR, et al. Quantitative and qualitative evalution of microcirculatory blood vessels of the posterior segment using OCT angiography. Kataraktal’naya i refraktsionnaya khirurgiya. 2015;15(3):4–9. (In Russ.)
  26. Tokayer J, Jia Y, Dhalla AH, Huang D. Blood flow velocity quantification using split-spectrum amplitude-decorrelation angiography with optical coherence tomography. Biomed Opt Express. 2013;4(10):1909–1924. doi: 10.1364/boe.4.001909
  27. Carpineto P, Mastropasqua R, Marchini G, et al. Reproducibility and repeatability of foveal avascular zone measurements in healthy subjects by optical coherence tomography angiography. Br J Ophthalmol. 2016;100(5):671–676. doi: 10.1136/bjophthalmol-2015-307330
  28. Lei J, Durbin MK, Shi Y, et al. Repeatability and reproducibility of superficial macular retinal vessel density measurements using optical coherence tomography angiography en face images. JAMA Ophthalmol. 2017;135(10):1092–1098. doi: 10.1001/jamaophthalmol.2017.3431
  29. Lee M, Kim K, Lim H, et al. Repeatability of vessel density measurements using optical coherence tomography angiography in retinal diseases. Br J Ophthalmol. 2019;103:704–710. doi: 10.1136/bjophthalmol-2018-312516
  30. Takase N, Nozaki M, Kato A, et al. Enlargement of foveal avascular zone in diabetic eyes evaluated by en face optical coherence tomography angiography. Retina. 2015;35(11):2377–2383. doi: 10.1097/IAE.0000000000000849
  31. Ho J, Dans K, You Q, et al. Comparison of 3 mm × 3 mm versus 6 mm × 6 mm optical coherence tomography angiography scan sizes in the evaluation of non-proliferative diabetic retinopathy. Retina. 2019;39(2):259–264. doi: 10.1097/IAE.0000000000001951
  32. Zhu Y, Cui Y, Wang JC, et al. Different scan protocols affect the detection rates of diabetic retinopathy lesions by wide-field swept-source optical coherence tomography angiography. Am J Ophthalmol. 2020;215:72–80. doi: 10.1016/j.ajo.2020.03.004
  33. Goudot MM, Sikorav A, Semoun O, et al. Parafoveal OCT angiography features in diabetic patients without clinical diabetic retinopathy: a qualitative and quantitative analysis. J Ophthalmol. 2017;2017:8676091. doi: 10.1155/2017/8676091
  34. Burnasheva MA, Kulikov AN, Maltsev DS. Personalized analysis of foveal avascular zone with optical coherence tomography angiography. Ophthalmology Journal. 2017;10(4):32–40. (In Russ.) doi: 10.17816/OV10432-40
  35. Choi W, Mohler KJ, Potsaid B, et al. Choriocapillaris and choroidal microvasculature imaging with ultrahigh speed OCT angiography. PLoS ONE. 2013;8(12): e81499. doi: 10.1371/journal.pone.0081499
  36. Johnson RN, Fu AD, McDonald HR., et al. Fluorescein angiography: basic principles and interpretation. In: Ryan SJ, Sadda SR, Hinton DR, eds. Retina. London: Elsevier Saunders; 2012. Vol. 1. P. 2–50. doi: 10.1016/B978-1-4557-0737-9.00001-1
  37. Cheung N, Mitchell P, Wong TY. Diabetic retinopathy. Lancet. 2010;376(9735):124–136. doi: 10.1016/S0140-6736(09)62124-3
  38. Bradley PD, Sim DA, Keane PA, et al The evaluation of diabetic macular ischemia using optical coherence tomography angiography. Invest Ophthalmol Vis Sci. 2016;57(2):626–631. doi: 10.1167/iovs.15-18034
  39. Bresnick GH, Condit R, Syrjala S, et al. Abnormalities of the foveal avascular zone in diabetic retinopathy. Arch Ophthalmol. 1984;102(9):1286–1293. doi: 10.1001/archopht.1984.01040031036019
  40. Parravano M, De Geronimo D, Scarinci F, et al. Diabetic microaneurysms internal reflectivity on spectral-domain optical coherence tomography and optical coherence tomography angiography detection. Am J Ophthalmol. 2017;179:90–96. doi: 10.1016/j.ajo.2017.04.021
  41. Salz DA, de Carlo TE, Adhi M, et al. Select features of diabetic retinopathy on swept-source optical coherence tomographic angiography compared with fluorescein angiography and normal eyes. JAMA Ophthalmol. 2016;134(6):644–650. doi: 10.1001/jamaophthalmol.2016.0600
  42. Giuffre C, Carnevali A, Cicinelli MV, et al. Optical coherence tomography angiography of venous loops in diabetic retinopathy. Ophthalmic Surg Lasers Imaging Retina. 2017;48(6):518–520. doi: 10.3928/23258160-20170601-13
  43. Arya M, Sorour O, Chaudhri J, et al. Distinguishing intraretinal microvascular abnormalities from retinal neovascularization using optical coherence tomography angiography. Retina. 2019;40(9):1686–1695. doi: 10.1097/IAE.0000000000002671
  44. Miwa Y, Murakami T, Suzuma K, et al. Relationship between functional and structural changes in diabetic vessels in optical coherence tomography angiography. Sci. Rep. 2016;6:29064. doi: 10.1038/srep29064
  45. Couturier A, Mane V, Bonnin S, et al. Capillary plexus anomalies in diabetic retinopathy on optical coherence tomography angiography. Retina. 2015;35(11):2384–2391. doi: 10.1097/IAE.0000000000000859
  46. Stanga PE, Papayannis A, Tsamis E, et al. New findings in diabetic maculopathy and proliferative disease by swept-source optical coherence tomography angiography. Dev. Ophthalmol. 2016;56:113–121. doi: 10.1159/000442802
  47. Shchuko AG, Akulenko MV, Bukina VV, Samsonov DYu. OCTA angiography in the complex diagnosis of preclinical forms of retinal neovascularization. Sovremennyye tekhnologii v oftal’mologii. 2019;(6): 151–156. (In Russ.) doi: 10.25276/2312-4911-2019-6-151-156
  48. Pan J, Chen D, Yang X, et al. Characteristics of neovascularization in early stages of proliferative diabetic retinopathy by optical coherence tomography angiography. American Journal of Ophthalmology. 2018;192:146–156. doi: 10.1016/j.ajo.2018.05.018
  49. Lin AD, Lee AY, Zhang Q, et al. Association between OCT-based microangiography perfusion indices and diabetic retinopathy severity. Br J Ophthalmol. 2017;101(7):960–964. doi: 10.1136/bjophthalmol-2016-309514
  50. Soares M, Neves C, Marques IP, et al. Comparison of diabetic retinopathy classification using fluorescein angiography and optical coherence tomography angiography. Br J Ophthalmol. 2017;101(1):62–68. doi: 10.1136/bjophthalmol-2016-309424
  51. Di G, Weihong Y, Xiao Z, et al. A morphological study of the foveal avascular zone in patients with diabetes mellitus using optical coherence tomography angiography. Graefes Arch Clin Exp Ophthalmol. 2016;254(5):873–879. doi: 10.1007/s00417-015-3143-7
  52. Sim DA, Keane P, Fung S, et al. Quantitative analysis of diabetic macular ischemia using optical coherence tomography. Invest Ophthalmol Vis Sci. 2014;55(1):417–423. doi: 10.1167/iovs.13-12677
  53. Cennamo G, Romano MR, Nicoletti G, et al. Optical coherence tomography angiography versus fluorescein angiography in the diagnosis of ischaemic diabetic maculopathy. Acta Ophthalmol. 2017;95(1): e36-e42. doi: 10.1111/aos.13159
  54. Arend O, Wolf S, Jung F, et al. Retinal microcirculation in patients with diabetes mellitus: dynamic and morphological analysis of perifoveal capillary network. Br J Ophthalmol. 1991;75(9):514–518. doi: 10.1136/bjo.75.9.514
  55. Agemy SA, Scripsema NK, Shah CM, et al. Retinal vascular perfusion density mapping using optical coherence tomography angiography in normals and diabetic retinopathy patients. Retina. 2015;35(11):2353–2363. doi: 10.1097/IAE.0000000000000862
  56. Conti FF, Qin VL, Rodrigues EB, et al. Choriocapillaris and retinal vascular plexus density of diabetic eyes using split-spectrum amplitude decorrelation spectral-domain optical coherence tomography angiography. Br J Ophthalmol. 2019;103(4):452–456. doi: 10.1136/bjophthalmol-2018-311903
  57. Fabrikantov OL, Pronichkina MM, Yablokova NV, Ovsyannikova NV. Innovative capabilities of non-invasive vital assessment of vascular status of microcirculatory bed in diabetic retinopathy. Vestnik Volgogradskogo gosudarstvennogo meditsinskogo universiteta. 2018;(4):41–45. (In Russ.) doi: 10.19163/1994-9480-2018-4(68)-41-45
  58. Aznabaev BM, Aleksandrov AA, Davletova RA, et al. Quantitative assessment of macular hemoperfusion in patients with nonproliferative diabetic retinopathy. Meditsinskiy vestnik Bashkortostana. 2019;14(3):5–9. (In Russ.)
  59. Kuehlewein L, Tepelus TC, An L, et al. Noninvasive visualization and analysis of the human parafoveal capillary network using swept source OCT optical microangiography. Invest Ophthalmol Vis Sci. 2015;56(6):3984–3988. doi: 10.1167/iovs.15-16510
  60. Krawitz BD, Mo S, Geyman LS, et al. Acircularity index and axis ratio of the foveal avascular zone in diabetic eyes and healthy controls measured by optical coherence tomography angiography. Vision Res. 2017;139:177–186. doi: 10.1016/j.visres.2016.09.019
  61. Provis JM, Hendrickson AE. The foveal avascular region of developing human retina. Arch Ophthalmol. 2008;126(4):507–511. doi: 10.1001/archopht.126.4.507
  62. Samara WA, Say EAT, Khoo CTL, et al. Correlation of foveal avascular zone size with foveal morphology in normal eyes using optical coherence tomography angiography. Retina. 2015;35(11):2188–2195. doi: 10.1097/IAE.0000000000000847
  63. Ahmad Fadzil M, Ngah NF, George TM, et al. Analysis of foveal avascular zone in colour fundus images for grading of diabetic retinopathy severity. Annu Int Conf IEEE Eng Med Biol Soc. 2010;2010:5632–5635. doi: 10.1109/IEMBS.2010.5628041
  64. Laatikainen L, Larinkari J. Capillary-free area of the fovea with advancing age. Invest Ophthalmol Vis Sci. 1977;16(12):1154–1157.
  65. Vujosevic S, Muraca A, Alkabes M, et al Early microvascular and neural changes in patients with type 1 and type 2 diabetes mellitus without clinical signs of diabetic retinopathy. Retina. 2019;39(3): 435–445. doi: 10.1097/IAE.0000000000001990
  66. Scarinci F, Nesper PL, Fawzi AA. Deep retinal capillary non-perfusion is associated with photoreceptor disruption in diabetic macular ischemia. Am J Ophthalmol. 2016;168:129–138. doi: 10.1016/j.ajo.2016.05.002
  67. Durbin MK, An L, Shemonski ND, et al. Quantification of retinal microvascular density in optical coherence tomographic angiography images in diabetic retinopathy. JAMA Ophthalmol. 2017;135(4):370–376. doi: 10.1001/jamaophthalmol.2017.0080
  68. Sandhu HS, Eladawi N, Elmogy M, et al. Automated diabetic retinopathy detection using optical coherence tomography angiography: a pilot study. Retinal Physician. 2018;102(11):1564–1569. doi: 10.1136/bjophthalmol-2017-311489
  69. Fabrikantov OL, Yablokova NV, Yablokov MM, Ovsyannikova NV. Examination of vessels in the macular area using oct-angiography before and after panretinal laser coagulation in diabetic retinopathy. Vestnik Volgogradskogo gosudarstvennogo meditsinskogo universiteta. 2018;(4):69–72. (In Russ.) doi: 10.19163/1994-9480-2018-4(68)-69-72
  70. Yablokova NV, Fabrikantov OL. Investigation of the influence of panretinal laser coagulation concerning diabetic retinopathy on the vascular system of the eye. Sovremennyye tekhnologii v oftal’mologii. 2019;(6):157–162. (In Russ.) doi: 10.25276/2312-4911-2019-6-157-162
  71. Neroev VV, Kiseleva TN, Okhotsimskaya TD, et al. Impact of antiangiogenic therapy on ocular blood flow and microcirculation in diabetic macular edema. Vestnik oftalmologii. 2018;134(4):3–10. (In Russ.) doi: 10.17116/oftalma20181340413
  72. Hirano T, Kakihara S, Toriyama Y, et al. Wide-field en face swept-source optical coherence tomography angiography using extended field imaging in diabetic retinopathy. Br J Ophthalmol. 2018;102(9):1199–1203. doi: 10.1136/bjophthalmol-2017-311358

Supplementary files

Supplementary Files
Action
1. JATS XML
Download

Copyright (c) 2021 Pomytkina N.V., Sorokin E.L.

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.
СМИ зарегистрировано Федеральной службой по надзору в сфере связи, информационных технологий и массовых коммуникаций (Роскомнадзор).
Регистрационный номер и дата принятия решения о регистрации СМИ: серия ПИ № ФС 77-65574 от 04 мая 2016 г.


This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies