Automated quantification of nonperfusion in three retinal plexuses using projection-resolved optical coherence tomography angiography in diabetic retinopathy

Investigative Ophthalmology and Visual Science

Volumn 57, Issue 13, 2016, Pages 5101-5106

  Zhang, Miao ^a   Hwang, Thomas S ^a   Dongye, Changlei ^a,b   Wilson, David J ^a   Huang, David ^a   Jia, Yali ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b SHANDONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Avascular area; Diabetic retinopathy; Optical coherence tomography angiography

Indexed keywords

ADULT; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DIABETIC RETINOPATHY; DIAGNOSTIC ACCURACY; FEMALE; FOVEAL AVASCULAR ZONE; GANGLION CELL LAYER; HUMAN; INNER LIMITING MEMBRANE; MALE; OPTICAL COHERENCE TOMOGRAPHIC ANGIOGRAPHY; PRIORITY JOURNAL; RECEIVER OPERATING CHARACTERISTIC; RETINA ANGIOGRAPHY; RETINA BLOOD FLOW; RETINA CAPILLARY; RETINAL INNER NUCLEAR LAYER; RETINAL INNER PLEXIFORM LAYER; RETINAL OUTER NUCLEAR LAYER; RETINAL OUTER PLEXIFORM LAYER; RETINAL PLEX; SENSITIVITY AND SPECIFICITY; AGED; ALGORITHM; DIAGNOSTIC IMAGING; EYE FUNDUS; FLUORESCENCE ANGIOGRAPHY; FOLLOW UP; MIDDLE AGED; OPTICAL COHERENCE TOMOGRAPHY; PROCEDURES; REPRODUCIBILITY; RETINA BLOOD VESSEL; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; ALGORITHMS; DIABETIC RETINOPATHY; FEMALE; FLUORESCEIN ANGIOGRAPHY; FOLLOW-UP STUDIES; FUNDUS OCULI; HUMANS; MALE; MIDDLE AGED; REPRODUCIBILITY OF RESULTS; RETINAL VESSELS; TOMOGRAPHY, OPTICAL COHERENCE;

EID: 85016067708     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.16-19776     Document Type: Article

References (41)

1. Congdon N, O’Colmain B, Klaver CC, et al.; for the Eye Diseases Prevalence Research Group. Causes and prevalence of visual impairment among adults in the United States. Arch Ophthalmol. 2004;122:477–485.
2. Panel AR. Preferred Practice Pattern, Diabetic Retinopathy. San Francisco, CA: American Academy of Ophthalmology; 2014:1–65.
3. Antonetti DA, Klein R, Gardner TW. Diabetic retinopathy. N Engl J Med. 2012;366:1227–1239.
4. Early Treatment Diabetic Retinopathy Study Research Group. Fluorescein angiographic risk factors for progression of diabetic retinopathy: ETDRS report number 13. Ophthalmology. 1991;98:834–840.
5. Early Treatment Diabetic Retinopathy Study Research Group. Classification of diabetic retinopathy from fluorescein angiograms: ETDRS report number 11. Ophthalmology. 1991;98: 807–822.
6. 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.
7. Hwang TS, Gao SS, Liu L, et al. Automated quantification of capillary nonperfusion using optical coherence tomography angiography in diabetic retinopathy. JAMA Ophthalmol. 2016; 134:367–373.
8. Hwang TS, Jia Y, Gao SS, et al. Optical coherence tomography angiography features of diabetic retinopathy. Retina (Phila-delphia, Pa). 2015;35:2371–2376.
9. Kuehlewein L, Tepelus TC, An L, Durbin MK, Srinivas S, Sadda SR. Noninvasive visualization and analysis of the human parafoveal capillary network using swept source OCT optical microangiography human parafoveal capillary network analysis. Invest Ophthalmol Vis Sci. 2015;56:3984–3988.
10. Kim DY, Fingler J, Zawadzki RJ, et al. Noninvasive imaging of the foveal avascular zone with high-speed, phase-variance optical coherence tomography. Invest Ophthalmol Vis Sci. 2012;53:85–92.
11. 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.
12. Spaide RF. Volume-rendered optical coherence tomography of diabetic retinopathy pilot study. Am J Ophthalmol. 2015;160: 1200–1210.
13. Matsunaga DR, Yi JJ, Koo LOD, 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.
14. Zhang M, Hwang TS, Campbell JP, et al. Projection-resolved optical coherence tomographic angiography. Biomed Optics Express. 2016;7:816–828.
15. Hwang TS, Zhang M, Bhavsar K, et al. Projection-resolved optical coherence tomography angiography visualizes capillary nonperfusion in three distinct retinal plexuses in diabetic retinopathy. JAMA Ophthalmol. In press.
16. Kurokawa K, Sasaki K, Makita S, Hong Y-J, Yasuno Y. Three-dimensional retinal and choroidal capillary imaging by power Doppler optical coherence angiography with adaptive optics. Opt Express. 2012;20:22796–22812.
17. 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.
18. Jia Y, Tan O, Tokayer J, et al. Split-spectrum amplitude-decorrelation angiography with optical coherence tomography. Optics Express. 2012;20:4710–4725.
19. Gao SS, Liu G, Huang D, Jia Y. Optimization of the split-spectrum amplitude-decorrelation angiography algorithm on a spectral optical coherence tomography system. Optics Lett. 2015;40:2305–2308.
20. Liu L, Jia Y, Takusagawa HL, et al. Optical coherence tomography angiography of the peripapillary retina in glaucoma. JAMA Ophthalmol. 2015;133:1045–1052.
21. Kraus MF, Potsaid B, Mayer MA, et al. Motion correction in optical coherence tomography volumes on a per A-scan basis using orthogonal scan patterns. Biomed Optics Express. 2012; 3:1182–1199.
22. Kraus MF, Liu JJ, Schottenhamml J, et al. Quantitative 3D-OCT motion correction with tilt and illumination correction, robust similarity measure and regularization. Biomed Optics Express. 2014;5:2591–2613.
23. Zhang M, Wang J, Pechauer AD, et al. Advanced image processing for optical coherence tomographic angiography of macular diseases. Biomed. Optics Express 2015;6:4661–4675.
24. Snodderly DM, Weinhaus RS, Choi J. Neural-vascular relationships in central retina of macaque monkeys (Macaca fascicularis). J Neurosci. 1992;12:1169–1193.
25. Snodderly DM, Weinhaus RS. Retinal vasculature of the fovea of the squirrel monkey, Saimiri sciureus: three-dimensional architecture, visual screening, and relationships to the neuronal layers. J Comp Neurol. 1990;297:145–163.
26. Gariano RF, Iruela-Arispe ML, Hendrickson AE. Vascular development in primate retina: comparison of laminar plexus formation in monkey and human. Invest Ophthalmol Vis Sci. 1994;35:3442–3455.
27. Chan G, Balaratnasingam C, Yu PK, et al. Quantitative morphometry of perifoveal capillary networks in the human retina. Invest Ophthalmol Vis Sci. 2012;53:5502–5514.
28. Tan PEZ, 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.
29. Frangi AF, Niessen WJ, Vincken KL, Viergever MA. Multiscale vessel enhancement filtering. In: WM Wells, Colchester A, Delp S, eds. Medical Image Computing and Computer-Assisted Interventation—MICCAI’98: First International Conference. Berlin: Springer; 1998:130–137.
30. Fraz MM, Remagnino P, Hoppe A, et al. Blood vessel segmentation methodologies in retinal images: a survey. Comput Methods Program Biomed. 2013;108:407–433.
31. Sofka M, Stewart CV. Retinal vessel centerline extraction using multiscale matched filters confidence and edge measures. IEEE Trans Med Imag. 2006;25:1531–1546.
32. Zhang HF, Maslov K, Li M-L, Stoica G, Wang LV. In vivo volumetric imaging of subcutaneous microvasculature by photoacoustic microscopy. Optics Express. 2006;14:9317–9323.
33. Zhang A, Zhang Q, Wang RK. Minimizing projection artifacts for accurate presentation of choroidal neovascularization in OCT micro-angiography. Biomed Optics Express. 2015;6: 4130–4143.
34. Zhang A, Wang RK. Feature space optical coherence tomography based micro-angiography. Biomed Optics Express. 2015;6:1919–1928.
35. Maurer CR, Rensheng Q, Raghavan V. A linear time algorithm for computing exact Euclidean distance transforms of binary images in arbitrary dimensions. IEEE Trans Pattern Anal Mach Intell. 2003;25:265–270.
36. Shimizu K, Ujiie K. Structure of Ocular Vessels. Tokyo, Japan: Igaku-Shoin Medical Publishers; 1978.
37. Huang D, Chopra V, Lu AT-H, Tan O, Francis B, Varma R. Does optic nerve head size variation affect circumpapillary retinal nerve fiber layer thickness measurement by optical coherence tomography? Disc size and RNFL layer thickness measurement by OCT. Invest Ophthalmol Vis Sci. 2012;53:4990–4997.
38. Mansour AM, Schachat A, Bodiford G, Haymond R. Foveal avascular zone in diabetes mellitus. Retina. 1993;13:125–128.
39. Bresnick GH, Condit R, Syrjala S, Palta M, Groo A, Korth K. Abnormalities of the foveal avascular zone in diabetic retinopathy. Arch Ophthalmol. 1984;102:1286–1293.
40. Yanni SE, Wang J, Chan M, et al. Foveal avascular zone and foveal pit formation after preterm birth. Br J Ophthalmol. 2012;96:961–966.
41. Silva PS, Cavallerano JD, Haddad NMN, et al. Peripheral lesions identified on ultrawide field imaging predict increased risk of diabetic retinopathy progression over 40 years. Ophthalmology. 2015;122:949–956.