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International Ophthalmology

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Open Access 01-10-2019 | Review

The diagnostic value of optical coherence tomography angiography in diabetic retinopathy: a systematic review

Author: David Gildea

Published in: International Ophthalmology | Issue 10/2019

Abstract

Purpose

Diabetic retinopathy (DR) is one of the leading causes of blindness worldwide. Accurate investigative tools are essential for the early diagnosis and monitoring of the disease. Optical coherence tomography angiography (OCTA) is a recently developed technology that enables visualisation of the retinal microvasculature.

Methods

A systematic review of the literature was performed to examine the diagnostic use of OCTA in DR to date. Medline, EMBASE, and Cochrane databases were searched to find relevant studies. Sixty-one original studies were selected for the review.

Results and discussion

OCTA has demonstrated the ability to identify microvascular features of DR such as microaneurysms, neovascularisation, and capillary non-perfusion. Furthermore, OCTA is enabling quantitative evaluation of the microvasculature of diabetic eyes. It has demonstrated the ability to detect early microvascular changes, in eyes with or without clinically evident DR. It has also been shown to detect progressive changes in the foveal avascular zone, and vascular perfusion density, with worsening severity of disease. It provides three-dimensional visualisation of the individual retinal vascular networks and is thereby enhancing our understanding of the role of the deeper vasculature in the pathogenesis of diabetic retinopathy and maculopathy.

Conclusion

However, limitations exist with current OCTA technology, in respect to the small field of view, image quality, projection artefact, and inaccuracies in analysis of the deeper vascular layers. While questions remain regarding its practical applicability in its present form, with continuing development and improvement of the technology, the diagnostic value of OCTA in diabetic retinopathy is likely to become evident.

Klein R, Klein BE, Moss SE, Davis MD, DeMets DL (1984) 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 (Chicago, Ill 1960) 102(4):527–532

Saaddine JB, Honeycutt AA, Narayan KMV, Zhang X, Klein R, Boyle JP (2008) Projection of diabetic retinopathy and other major eye diseases among people with diabetes mellitus: United States, 2005–2050. Arch Ophthalmol (Chicago, Ill 1960) 126(12):1740–1747

Yannuzzi LA, Rohrer KT, Tindel LJ, Sobel RS, Costanza MA, Shields W et al (1986) Fluorescein angiography complication survey. Ophthalmology 93(5):611–617PubMed

Ishibazawa A, Nagaoka T, Takahashi A, Omae T, Tani T, Sogawa K et al (2015) Optical coherence tomography angiography in diabetic retinopathy: a prospective pilot study. Am J Ophthalmol 160(1):35–44PubMed

Moher D, Shamseer L, Clarke M, Ghersi D, Liberati A, Petticrew M et al (2015) Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev 4:1PubMedPubMedCentral

Couturier A, Mane V, Bonnin S, Erginay A, Massin P, Gaudric A et al (2015) Capillary plexus anomalies in diabetic retinopathy on optical coherence tomography angiography. Retina 35(11):2384–2391PubMed

Tokayer J, Jia Y, Dhalla A-H, Huang D (2013) Blood flow velocity quantification using split-spectrum amplitude-decorrelation angiography with optical coherence tomography. Biomed Opt Express 4(10):1909–1924PubMedPubMedCentral

Parravano M, De Geronimo D, Scarinci F, Querques L, Virgili G, Simonett JM et al (2017) Relationship between internal reflectivity of diabetic microaneurysms on SD-OCT and detection on OCT angiography. Am J Ophthalmol 179:90–96PubMed

Miwa Y, Murakami T, Suzuma K, Uji A, Yoshitake S, Fujimoto M et al (2016) Relationship between functional and structural changes in diabetic vessels in optical coherence tomography angiography. Sci Rep 6:29064PubMedPubMedCentral

10.

Hasegawa N, Nozaki M, Takase N, Yoshida M, Ogura Y (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(9):OCT348–OCT355PubMed

11.

Peres MB, Kato RT, Kniggendorf VF, Cole ED, Onal S, Torres E et al (2016) Comparison of optical coherence tomography angiography and fluorescein angiography for the identification of retinal vascular changes in eyes with diabetic macular edema. Ophthalmic Surg Lasers Imaging Retina 47(11):1013–1019PubMed

12.

Salz DA, de Carlo TE, Adhi M, Moult E, Choi W, Baumal CR et al (2016) Select features of diabetic retinopathy on swept-source optical coherence tomographic angiography compared with fluorescein angiography and normal eyes. JAMA Ophthalmol 134(6):644–650PubMedPubMedCentral

13.

Jia Y, Bailey ST, Hwang TS, McClintic SM, Gao SS, Pennesi ME et al (2015) Quantitative optical coherence tomography angiography of vascular abnormalities in the living human eye. Proc Natl Acad Sci U S A 112(18):E2395–E2402PubMedPubMedCentral

14.

Savastano MC, Federici M, Falsini B, Caporossi A, Minnella AM (2016) Detecting papillary neovascularization in proliferative diabetic retinopathy using optical coherence tomography angiography. Acta Ophthalmol. 30:353–359

15.

Zhang M, Wang J, Pechauer AD, Hwang TS, Gao SS, Liu L et al (2015) Advanced image processing for optical coherence tomographic angiography of macular diseases. Biomed Opt Express 6(12):4661–4675PubMedPubMedCentral

16.

de Carlo TE, Bonini Filho MA, Baumal CR, Reichel E, Rogers A, Witkin AJ et al (2016) Evaluation of preretinal neovascularization in proliferative diabetic retinopathy using optical coherence tomography angiography. Ophthalmic Surg Lasers Imaging Retina 47(2):115–119PubMed

17.

Ishibazawa A, Nagaoka T, Yokota H, Takahashi A, Omae T, Song Y-S et al (2016) Characteristics of retinal neovascularization in proliferative diabetic retinopathy imaged by optical coherence tomography angiography. Invest Ophthalmol Vis Sci 57(14):6247–6255PubMed

18.

Singh A, Agarwal A, Mahajan S, Karkhur S, Singh R, Bansal R et al (2017) Morphological differences between optic disc collaterals and neovascularization on optical coherence tomography angiography. Graefes Arch Clin Exp Ophthalmol 255(4):753–759PubMed

19.

Takase N, Nozaki M, Kato A, Ozeki H, Yoshida M, Ogura Y (2015) Enlargement of foveal avascular zone in diabetic eyes evaluated by en face optical coherence tomography angiography. Retina 35(11):2377–2383PubMed

20.

Dimitrova G, Chihara E, Takahashi H, Amano H, Okazaki K (2017) Quantitative retinal optical coherence tomography angiography in patients with diabetes without diabetic retinopathy. Invest Ophthalmol Vis Sci 58(1):190–196PubMed

21.

de Carlo TE, Chin AT, Bonini Filho MA, Adhi M, Branchini L, Salz DA 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(11):2364–2370PubMed

22.

Di G, Weihong Y, Xiao Z, Zhikun Y, Xuan Z, Yi Q et al (2016) A morphological study of the foveal avascular zone in patients with diabetes mellitus using optical coherence tomography angiography. Graefes Arch Clin Exp Ophthalmol 254(5):873–879PubMed

23.

Al-Sheikh M, Akil H, Pfau M, Sadda SR (2016) Swept-Source OCT angiography imaging of the foveal avascular zone and macular capillary network density in diabetic retinopathy. Invest Ophthalmol Vis Sci 57(8):3907–3913PubMed

24.

Gozlan J, Ingrand P, Lichtwitz O, Cazet-Supervielle A, Benoudis L, Boissonnot M et al (2017) Retinal microvascular alterations related to diabetes assessed by optical coherence tomography angiography: a cross-sectional analysis. Medicine (Baltimore) 96(15):e6427

25.

Balaratnasingam C, Inoue M, Ahn S, McCann J, Dhrami-Gavazi E, Yannuzzi LA et al (2016) Visual acuity is correlated with the area of the foveal avascular zone in diabetic retinopathy and retinal vein occlusion. Ophthalmology 123(11):2352–2367PubMed

26.

Yu S, Lu J, Cao D, Liu R, Liu B, Li T et al (2016) The role of optical coherence tomography angiography in fundus vascular abnormalities. BMC Ophthalmol 16:107PubMedPubMedCentral

27.

Samara WA, Shahlaee A, Adam MK, Khan MA, Chiang A, Maguire JI et al (2017) Quantification of diabetic macular ischemia using optical coherence tomography angiography and its relationship with visual acuity. Ophthalmology 124(2):235–244PubMed

28.

Simonett JM, Scarinci F, Picconi F, Giorno P, De Geronimo D, Di Renzo A et al (2017) Early microvascular retinal changes in optical coherence tomography angiography in patients with type 1 diabetes mellitus. Acta Ophthalmol 95:e751–e755PubMed

29.

Hwang TS, Gao SS, Liu L, Lauer AK, Bailey ST, Flaxel CJ et al (2016) Automated quantification of capillary nonperfusion using optical coherence tomography angiography in diabetic retinopathy. JAMA Ophthalmol 134(4):367–373PubMedPubMedCentral

30.

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 27:716–729PubMed

31.

Durbin MK, An L, Shemonski ND, Soares M, Santos T, Lopes M et al (2017) Quantification of retinal microvascular density in optical coherence tomographic angiography images in diabetic retinopathy. JAMA Ophthalmol 135(4):370–376PubMedPubMedCentral

32.

Carnevali A, Sacconi R, Corbelli E, Tomasso L, Querques L, Zerbini G 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 54:695–702PubMed

33.

Bhanushali D, Anegondi N, Gadde SGK, Srinivasan P, Chidambara L, Yadav NK et al (2016) Linking retinal microvasculature features with severity of diabetic retinopathy using optical coherence tomography angiography. Invest Ophthalmol Vis Sci 57(9):OCT519–OCT525PubMed

34.

Lee H, Lee M, Chung H, Kim HC (2017) Quantification of retinal vessel tortuosity in diabetic retinopathy using optical coherence tomography angiography. Retina 38:1

35.

Krawitz BD, Mo S, Geyman LS, Agemy SA, Scripsema NK, Garcia PM et al (2017) Acircularity index and axis ratio of the foveal avascular zone in diabetic eyes and healthy controls measured by optical coherence tomography angiography. Vis Res 139:177–186PubMed

36.

Freiberg FJ, Pfau M, Wons J, Wirth MA, Becker MD, Michels S (2016) Optical coherence tomography angiography of the foveal avascular zone in diabetic retinopathy. Graefes Arch Clin Exp Ophthalmol 254(6):1051–1058PubMed

37.

Agemy SA, Scripsema NK, Shah CM, Chui T, Garcia PM, Lee JG et al (2015) Retinal vascular perfusion density mapping using optical coherence tomography angiography in normals and diabetic retinopathy patients. Retina 35(11):2353–2363PubMed

38.

Spaide RF, Fujimoto JG, Waheed NK (2015) Image artifacts in optical coherence tomography angiography. Retina 35(11):2163–2180PubMedPubMedCentral

39.

Kim AY, Chu Z, Shahidzadeh A, Wang RK, Puliafito CA, Kashani AH (2016) Quantifying microvascular density and morphology in diabetic retinopathy using spectral-domain optical coherence tomography angiography. Invest Ophthalmol Vis Sci 57(9):OCT362–OCT370PubMedPubMedCentral

40.

You Q, Freeman WR, Weinreb RN, Zangwill L, Manalastas PIC, Saunders LJ et al (2016) Reproducibility of vessel density measurement with optical coherence tomography angiography in eyes with and without retinopathy. Retina 37(8):1475–1482

41.

Ting DSW, Tan GSW, Agrawal R, Yanagi Y, Sie NM, Wong CW et al (2017) Optical coherence tomographic angiography in type 2 diabetes and diabetic retinopathy. JAMA Ophthalmol 135(4):306–312PubMed

42.

Zahid S, Dolz-Marco R, Freund KB, Balaratnasingam C, Dansingani K, Gilani F et al (2016) Fractal dimensional analysis of optical coherence tomography angiography in eyes with diabetic retinopathy. Invest Ophthalmol Vis Sci 57(11):4940–4947PubMed

43.

Minnella AM, Savastano MC, Federici M, Falsini B, Caporossi A (2016) Superficial and deep vascular structure of the retina in diabetic macular ischaemia: OCT angiography. Acta Ophthalmol 96(5):e647–e648PubMed

44.

Scarinci F, Nesper PL, Fawzi AA (2016) Deep retinal capillary nonperfusion is associated with photoreceptor disruption in diabetic macular ischemia. Am J Ophthalmol 168:129–138PubMedPubMedCentral

45.

Bradley PD, Sim DA, Keane PA, Cardoso J, Agrawal R, Tufail A et al (2016) The evaluation of diabetic macular ischemia using optical coherence tomography angiography. Invest Ophthalmol Vis Sci 57(2):626–631PubMed

46.

Hwang TS, Jia Y, Gao SS, Bailey ST, Lauer AK, Flaxel CJ et al (2015) Optical coherence tomography angiography features of diabetic retinopathy. Retina 35(11):2371–2376PubMedPubMedCentral

47.

Soares M, Neves C, Marques IP, Pires I, Schwartz C, Costa MA et al (2017) Comparison of diabetic retinopathy classification using fluorescein angiography and optical coherence tomography angiography. Br J Ophthalmol 101(1):62–68PubMed

48.

Cennamo G, Romano MR, Nicoletti G, Velotti N, de Crecchio G (2017) Optical coherence tomography angiography versus fluorescein angiography in the diagnosis of ischaemic diabetic maculopathy. Acta Ophthalmol 95(1):e36–e42PubMed

49.

Early Treatment Diabetic Retinopathy Study Research Group (1991) Classification of diabetic retinopathy from fluorescein angiograms. ETDRS report number 11. Ophthalmology 98(5 Suppl):807–822

50.

Mao L, Weng S-S, Gong Y-Y, Yu S-Q (2017) Optical coherence tomography angiography of macular telangiectasia type 1: comparison with mild diabetic macular edema. Lasers Surg Med 49(3):225–232PubMed

51.

Lee J, Moon BG, Cho AR, Yoon YH (2016) Optical coherence tomography angiography of DME and its association with anti-VEGF treatment response. Ophthalmology 123(11):2368–2375PubMed

52.

de Carlo TE, Chin AT, Joseph T, Baumal CR, Witkin AJ, Duker JS et al (2016) Distinguishing diabetic macular edema from capillary nonperfusion using optical coherence tomography angiography. Ophthalmic Surg Lasers Imaging Retina 47(2):108–114PubMed

53.

Mane V, Dupas B, Gaudric A, Bonnin S, Pedinielli A, Bousquet E et al (2016) Correlation between cystoid spaces in chronic diabetic macular edema and capillary nonperfusion detected by optical coherence tomography angiography. Retina 36:S102–S110PubMed

54.

Ghasemi Falavarjani K, Iafe NA, Hubschman J-P, Tsui I, Sadda SR, Sarraf D (2017) Optical coherence tomography angiography analysis of the foveal avascular zone and macular vessel density after anti-VEGF therapy in eyes with diabetic macular edema and retinal vein occlusion. Invest Ophthalmol Vis Sci 58(1):30–34PubMed

55.

Park JJ, Soetikno BT, Fawzi AA (2016) Characterization of the middle capillary plexus using optical coherence tomography angiography in healthy and diabetic eyes. Retina 36(11):2039–2050PubMedPubMedCentral

56.

Hwang TS, Zhang M, Bhavsar K, Zhang X, Campbell JP, Lin P et al (2016) Visualization of 3 distinct retinal plexuses by projection-resolved optical coherence tomography angiography in diabetic retinopathy. JAMA Ophthalmol 134(12):1411–1419PubMedPubMedCentral

57.

Zhang M, Hwang TS, Dongye C, Wilson DJ, Huang D, Jia Y (2016) Automated quantification of nonperfusion in three retinal plexuses using projection-resolved optical coherence tomography angiography in diabetic retinopathy. Invest Ophthalmol Vis Sci 57(13):5101–5106PubMedPubMedCentral

58.

Dongye C, Zhang M, Hwang TS, Wang J, Gao SS, Liu L et al (2017) Automated detection of dilated capillaries on optical coherence tomography angiography. Biomed Opt Express 8(2):1101–1109PubMedPubMedCentral

59.

Matsunaga DR, Yi JJ, De Koo LO, Ameri H, Puliafito CA, Kashani AH (2015) Optical coherence tomography angiography of diabetic retinopathy in human subjects. Ophthalmic Surg Lasers Imaging Retina 46(8):796–805PubMed

60.

Choi W, Waheed NK, Moult EM, Adhi M, Lee B, De Carlo T et al (2017) Ultrahigh speed swept source optical coherence tomography angiography of retinal and choriocapillaris alterations in diabetic patients with and without retinopathy. Retina 37(1):11–21PubMedPubMedCentral

61.

Stanga PE, Papayannis A, Tsamis E, Stringa F, Cole T, D’Souza Y et al (2016) New findings in diabetic maculopathy and proliferative disease by swept-source optical coherence tomography angiography. Dev Ophthalmol 56:113–121PubMed

62.

Zhang M, Hwang TS, Campbell JP, Bailey ST, Wilson DJ, Huang D et al (2016) Projection-resolved optical coherence tomographic angiography. Biomed Opt Express 7(3):816–828PubMedPubMedCentral

63.

Ploner SB, Moult EM, Choi W, Waheed NK, Lee B, Novais EA et al (2016) Toward quantitative optical coherence tomography angiography: visualizing blood flow speeds in ocular pathology using variable interscan time analysis. Retina 36(Suppl 1):S118–S126PubMedPubMedCentral

64.

Schottenhamml J, Moult EM, Ploner S, Lee B, Novais EA, Cole E et al (2016) An automatic, intercapillary area-based algorithm for quantifying diabetes-related capillary dropout using optical coherence tomography angiography. Retina 36(Suppl 1):S93–S101PubMedPubMedCentral

65.

Mo S, Krawitz B, Efstathiadis E, Geyman L, Weitz R, Chui TYP et al (2016) Imaging foveal microvasculature: optical coherence tomography angiography versus adaptive optics scanning light ophthalmoscope fluorescein angiography. Invest Ophthalmol Vis Sci. 57(9):OCT130–OCT140PubMedPubMedCentral

Title: The diagnostic value of optical coherence tomography angiography in diabetic retinopathy: a systematic review
Author: David Gildea
Publication date: 01-10-2019
Publisher: Springer Netherlands
Published in: International Ophthalmology / Issue 10/2019
Print ISSN: 0165-5701
Electronic ISSN: 1573-2630
DOI: https://doi.org/10.1007/s10792-018-1034-8

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

The diagnostic value of optical coherence tomography angiography in diabetic retinopathy: a systematic review

Abstract

Purpose

Methods

Results and discussion

Conclusion

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Purpose

Methods

Results and discussion

Conclusion

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