Quantifying microvascular density and morphology in diabetic retinopathy using spectral-domain optical coherence tomography angiography

Investigative Ophthalmology and Visual Science

Volumn 57, Issue 9, 2016, Pages OCT362-OCT370

  Kim, Alice Y ^a   Chu, Zhongdi ^b   Shahidzadeh, Anoush ^a   Wang, Ruikang K ^b   Puliafito, Carmen A ^a   Kashani, Amir H ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Diabetic retinopathy; Optical coherence tomography angiography; Quantitative analysis; Vessel density; Vessel morphology

Indexed keywords

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DIABETIC MACULAR EDEMA; DIABETIC RETINOPATHY; DISEASE SEVERITY; FEMALE; HUMAN; HUMAN TISSUE; INNER MEMBRANE; MALE; MEASUREMENT REPEATABILITY; PIGMENT EPITHELIUM; PRIORITY JOURNAL; RETINA ANGIOGRAPHY; RETINA BLOOD VESSEL; RETROSPECTIVE STUDY; SENSORY SYSTEM PARAMETERS; SKELETON DENSITY; SPECTRAL DOMAIN OPTICAL COHERENCE TOMOGRAPHY; VESSEL DENSITY; VESSEL DIAMETER INDEX; WHILE VESSEL MORPHOLOGY; AGED; ALGORITHM; CAPILLARY; CLINICAL TRIAL; COMPLICATION; EYE FUNDUS; FLUORESCENCE ANGIOGRAPHY; FOLLOW UP; MACULAR EDEMA; MIDDLE AGED; MULTICENTER STUDY; OPTICAL COHERENCE TOMOGRAPHY; PATHOLOGY; PATHOPHYSIOLOGY; PROCEDURES; REPRODUCIBILITY; SEVERITY OF ILLNESS INDEX;

ADULT; AGED; ALGORITHMS; CAPILLARIES; CROSS-SECTIONAL STUDIES; DIABETIC RETINOPATHY; FEMALE; FLUORESCEIN ANGIOGRAPHY; FOLLOW-UP STUDIES; FUNDUS OCULI; HUMANS; MACULAR EDEMA; MALE; MIDDLE AGED; REPRODUCIBILITY OF RESULTS; RETINAL VESSELS; RETROSPECTIVE STUDIES; SEVERITY OF ILLNESS INDEX; TOMOGRAPHY, OPTICAL COHERENCE;

EID: 84978518688     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.15-18904     Document Type: Article

References (45)

1. Klein BE. Overview of epidemiologic studies of diabetic retinopathy. Ophthalmic Epidemiol. 2007; 14: 179-183.
2. Klein R, Klein BE, Moss SE, Davis MD, DeMets DL. The Wisconsin epidemiologic study of diabetic retinopathy, II: prevalence and risk of diabetic retinopathy when age at diagnosis is less than 30 years. Arch Ophthalmol. 1984; 102: 520-526.
3. Klein R, Klein BE, Moss SE, Davis MD, DeMets DL. 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. 1984; 102: 527-532.
4. Matsunaga D, Yi J, Puliafito CA, Kashani AH. OCT angiography in healthy human subjects. Ophthalmic Surg Lasers Imaging Retina. 2014; 45: 510-515.
5. Spaide RF, Klancnik JM Jr, Cooney MJ. Retinal vascular layers imaged by fluorescein angiography and optical coherence tomography angiography. JAMA Ophthalmol. 2015; 133: 45-50.
6. Teussink MM, Breukink MB, van Grinsven MJ, et al. OCT angiography compared to fluorescein and indocyanine green angiography in chronic central serous chorioretinopathy. Invest Ophthalmol Vis Sci. 2015; 56: 5229-5237.
7. Mendis KR, Balaratnasingam C, Yu P, et al. Correlation of histologic and clinical images to determine the diagnostic value of fluorescein angiography for studying retinal capillary detail. Invest Ophthalmol Vis Sci. 2010; 51: 5864-5869.
8. Savastano MC, Lumbroso B, Rispoli M. In vivo characterization of retinal vascularization morphology using optical coherence tomography angiography. Retina. 2015; 35: 2196-2203.
9. 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: 2364-2370.
10. Matsunaga DR, Yi JJ, De Koo LO, Ameri H, Puliafito CA, Kashani AH. Optical coherence tomography angiography of diabetic retinopathy in human subjects. Ophthalmic Surg Lasers Imaging Retina. 2015; 46: 796-805.
11. Couturier A, Mane V, Bonnin S, et al. Capillary plexus anomalies in diabetic retinopathy on optical coherence tomography angiography. Retina. 2015; 35: 2384-2391.
12. Ishibazawa A, Nagaoka T, Takahashi A, et al. Optical coherence tomography angiography in diabetic retinopathy: a prospective pilot study. Am J Ophthalmol. 2015; 160: 35-44. e31.
13. Hwang TS, Jia Y, Gao SS, et al. Optical coherence tomography angiography features of diabetic retinopathy. Retina. 2015; 35: 2371-2376.
14. Kashani AH, Lee SY, Moshfeghi A, Durbin MK, Puliafito CA. Optical coherence tomography angiography of retinal venous occlusion. Retina. 2015; 35: 2323-2331.
15. Parsons-Wingerter P, Radhakrishnan K, Vickerman MB, Kaiser PK. Oscillation of angiogenesis with vascular dropout in diabetic retinopathy by VESsel GENeration analysis (VESGEN). Invest Ophthalmol Vis Sci. 2010; 51: 498-507.
16. Grauslund J, Green A, Kawasaki R, Hodgson L, Sjolie AK, Wong TY. Retinal vascular fractals and microvascular and macrovascular complications in type 1 diabetes. Ophthalmology. 2010; 117: 1400-1405.
17. Avakian A, Kalina RE, Sage EH, et al. Fractal analysis of regionbased vascular change in the normal and non-proliferative diabetic retina. Curr Eye Res. 2002; 24: 274-280.
18. Cheung N, Donaghue KC, Liew G, et al. Quantitative assessment of early diabetic retinopathy using fractal analysis. Diabetes Care. 2009; 32: 106-110.
19. Kunicki AC, Oliveira AJ, Mendonca MB, Barbosa CT, Nogueira RA. Can the fractal dimension be applied for the early diagnosis of non-proliferative diabetic retinopathy? Braz J Med Biol Res. 2009; 42: 930-934.
20. Cheung CY, Lamoureux E, Ikram MK, et al. Retinal vascular geometry in Asian persons with diabetes and retinopathy. J Diabetes Sci Technol. 2012; 6: 595-605.
21. Yau JW, Kawasaki R, Islam FM, et al. Retinal fractal dimension is increased in persons with diabetes but not impaired glucose metabolism: the Australian Diabetes, Obesity and Lifestyle (AusDiab) study. Diabetologia. 2010; 53: 2042-2045.
22. Lim SW, Cheung N, Wang JJ, et al. Retinal vascular fractal dimension and risk of early diabetic retinopathy: a prospective study of children and adolescents with type 1 diabetes. Diabetes Care. 2009; 32: 2081-2083.
23. Cheng SC, Huang YM. A novel approach to diagnose diabetes based on the fractal characteristics of retinal images. IEEE Trans Inf Technol Biomed. 2003; 7: 163-170.
24. Yu J, Jiang C, Wang X, et al. Macular perfusion in healthy Chinese: an optical coherence tomography angiogram study. Invest Ophthalmol Vis Sci. 2015; 56: 3212-3217.
25. Jia Y, Morrison JC, Tokayer J, et al. Quantitative OCT angiography of optic nerve head blood flow. Biomed Opt Express. 2012; 3: 3127-3137.
26. Jia Y, Bailey ST, Wilson DJ, et al. Quantitative optical coherence tomography angiography of choroidal neovascularization in age-related macular degeneration. Ophthalmology. 2014; 121: 1435-1444.
27. Jia Y, Bailey ST, Hwang TS, et al. Quantitative optical coherence tomography angiography of vascular abnormalities in the living human eye. Proc Natl Acad Sci U S A. 2015; 112: E2395-E2402.
28. Kuehlewein L, Sadda SR, Sarraf D. OCT angiography and sequential quantitative analysis of type 2 neovascularization after ranibizumab therapy. Eye (Lond). 2015; 29: 932-935.
29. Coscas G, Lupidi M, Coscas F, Francais C, Cagini C, Souied EH. Optical coherence tomography angiography during follow-up: qualitative and quantitative analysis of mixed type I and II choroidal neovascularization after vascular endothelial growth factor trap therapy. Ophthalmic Res. 2015; 54: 57-63.
30. Takase N, Nozaki M, Kato A, Ozeki H, Yoshida M, Ogura Y. Enlargement of foveal avascular zone in diabetic eyes evaluated by en face optical coherence tomography angiography. Retina. 2015; 35: 2377-2383.
31. 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 [published online ahead of print September 7, 2015]. Graefes Arch Clin Exp Ophthalmol. doi: 10.1007/s00417-015-3143-7.
32. Freiberg FJ, Pfau M, Wons J, Wirth MA, Becker MD, Michels S. Optical coherence tomography angiography of the foveal avascular zone in diabetic retinopathy [published online ahead of print September 4, 2015]. Graefes Arch Clin Exp Ophthalmol. doi: 10.1007/s00417-015-3148-2.
33. Hwang TS, Gao SS, Liu L, et al. Automated quantification of capillary nonperfusion using optical coherence tomography angiography in diabetic retinopathy. JAMA Ophthalmol. 2016: 1-7.
34. 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: 2353-2363.
35. Reif R, Qin J, An L, Zhi Z, Dziennis S, Wang R. Quantifying optical microangiography images obtained from a spectral domain optical coherence tomography system. Int J Biomed Imaging. 2012; 2012: 509783.
36. Grading diabetic retinopathy from stereoscopic color fundus photographs—an extension of the modified Airlie House classification: ETDRS report number 10: Early Treatment Diabetic Retinopathy Study Research Group. Ophthalmology. 1991; 98: 786-806.
37. Classification of diabetic retinopathy from fluorescein angiograms: ETDRS report number 11: Early Treatment Diabetic Retinopathy Study Research Group. Ophthalmology. 1991; 98: 807-822.
38. Tan PE, Yu PK, Balaratnasingam C, et al. Quantitative confocal imaging of the retinal microvasculature in the human retina. Invest Ophthalmol Vis Sci. 2012; 53: 5728-5736.
39. Jia Y, Tan O, Tokayer J, et al. Split-spectrum amplitudedecorrelation angiography with optical coherence tomography. Opt Express. 2012; 20: 4710-4725.
40. Zhang A, Zhang Q, Wang RK. Minimizing projection artifacts for accurate presentation of choroidal neovascularization in OCT micro-angiography. Biomed Opt Express. 2015; 6: 4130-4143.
41. Wiley HE, Ferris FL III. Nonproliferative diabetic retinopathy and diabetic macular edema. In: Ryan SJSS, Hinton DR, ed. Retina. London: Elsevier Saunders; 2013: 940-968.
42. Wilkinson CP, Ferris FL III, Klein RE, et al. Proposed international clinical diabetic retinopathy and diabetic macular edema disease severity scales. Ophthalmology. 2003; 110: 1677-1682.
43. Murakami T, Yoshimura N. Structural changes in individual retinal layers in diabetic macular edema. J Diabetes Res. 2013; 2013: 920713.
44. Otani T, Kishi S. Correlation between optical coherence tomography and fluorescein angiography findings in diabetic macular edema. Ophthalmology. 2007; 114: 104-107.
45. Bolz M, Ritter M, Schneider M, Simader C, Scholda C, Schmidt-Erfurth U. A systematic correlation of angiography and highresolution optical coherence tomography in diabetic macular edema. Ophthalmology. 2009; 116: 66-72.