Abstract

Diabetic retinopathy is a pathology where microvascular circulation abnormalities ultimately result in photoreceptor disruption and, consequently, permanent loss of vision. Here, we developed a method that automatically detects photoreceptor disruption in mild diabetic retinopathy by mapping ellipsoid zone reflectance abnormalities from en face optical coherence tomography images. The algorithm uses a fuzzy c-means scheme with a redefined membership function to assign a defect severity level on each pixel and generate a probability map of defect category affiliation. A novel scheme of unsupervised clustering optimization allows accurate detection of the affected area. The achieved accuracy, sensitivity and specificity were about 90% on a population of thirteen diseased subjects. This method shows potential for accurate and fast detection of early biomarkers in diabetic retinopathy evolution.

© 2017 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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2017 (10)

A. P. Runkle, P. K. Kaiser, S. K. Srivastava, A. P. Schachat, J. L. Reese, and J. P. Ehlers, “OCT Angiography and Ellipsoid Zone Mapping of Macular Telangiectasia Type 2 From the AVATAR Study,” Invest. Ophthalmol. Vis. Sci. 58(9), 3683–3689 (2017).
[PubMed]

D. Mukherjee, E. M. Lad, R. R. Vann, S. J. Jaffe, T. E. Clemons, M. Friedlander, E. Y. Chew, G. J. Jaffe, S. Farsiu, and MacTel Study Group, “Correlation Between Macular Integrity Assessment and Optical Coherence Tomography Imaging of Ellipsoid Zone in Macular Telangiectasia Type 2,” Invest. Ophthalmol. Vis. Sci. 58(6), BIO291 (2017).
[PubMed]

M. G. Kanakis, K. Giannouli, K. Andreanos, D. Papaconstantinou, C. Koutsandrea, I. Ladas, I. Georgalas, P. Petrou, and A. I. Kotsolis, “Capillary nonperfusion and photoreceptor loss in branch retinal vein occlusion: Spatial Correlation and Morphologic Characteristics,” Retina 37(9), 1710–1722 (2017).
[PubMed]

R. Zhao, A. Camino, J. Wang, A. M. Hagag, Y. Lu, S. T. Bailey, C. J. Flaxel, T. S. Hwang, D. Huang, D. Li, and Y. Jia, “Automated drusen detection in dry age-related macular degeneration by multiple-depth, en face optical coherence tomography,” Biomed. Opt. Express 8, 5049–5064 (2017).

Q. Chen, S. Huang, Q. Ma, H. Lin, M. Pan, X. Liu, F. Lu, and M. Shen, “Ultra-high resolution profiles of macular intra-retinal layer thicknesses and associations with visual field defects in primary open angle glaucoma,” Sci. Rep. 7, 41100 (2017).
[PubMed]

P. Zang, S. S. Gao, T. S. Hwang, C. J. Flaxel, D. J. Wilson, J. C. Morrison, D. Huang, D. Li, and Y. Jia, “Automated boundary detection of the optic disc and layer segmentation of the peripapillary retina in volumetric structural and angiographic optical coherence tomography,” Biomed. Opt. Express 8(3), 1306–1318 (2017).
[PubMed]

J. Wang, M. Zhang, T. S. Hwang, S. T. Bailey, D. Huang, D. J. Wilson, and Y. Jia, “Reflectance-based projection-resolved optical coherence tomography angiography [Invited],” Biomed. Opt. Express 8(3), 1536–1548 (2017).
[PubMed]

A. Montuoro, S. M. Waldstein, B. S. Gerendas, U. Schmidt-Erfurth, and H. Bogunović, “Joint retinal layer and fluid segmentation in OCT scans of eyes with severe macular edema using unsupervised representation and auto-context,” Biomed. Opt. Express 8(3), 1874–1888 (2017).
[PubMed]

L. Fang, D. Cunefare, C. Wang, R. H. Guymer, S. Li, and S. Farsiu, “Automatic segmentation of nine retinal layer boundaries in OCT images of non-exudative AMD patients using deep learning and graph search,” Biomed. Opt. Express 8(5), 2732–2744 (2017).
[PubMed]

L. W. Sun, J. Carroll, and B. J. Lujan, “Photoreceptor disruption and vision loss associated with central serous retinopathy,” American Journal of Ophthalmology Case Reports 8, 74–77 (2017).

2016 (10)

M. Ren, P. Liu, Z. Wang, and J. Yi, “A Self-Adaptive Fuzzy c-Means Algorithm for Determining the Optimal Number of Clusters,” Comput. Intell. Neurosci. 2016, 2647389 (2016).
[PubMed]

M. Zhang, T. S. Hwang, J. P. Campbell, S. T. Bailey, D. J. Wilson, D. Huang, and Y. Jia, “Projection-resolved optical coherence tomographic angiography,” Biomed. Opt. Express 7(3), 816–828 (2016).
[PubMed]

D. M. Sampson, D. Alonso-Caneiro, A. L. Chew, T. Lamey, T. McLaren, J. De Roach, and F. K. Chen, “Enhanced Visualization of Subtle Outer Retinal Pathology by En Face Optical Coherence Tomography and Correlation with Multi-Modal Imaging,” PLoS One 11(12), e0168275 (2016).
[PubMed]

V. S. Gattani, K. K. Vupparaboina, A. Patil, J. Chhablani, A. Richhariya, and S. Jana, “Semi-automated quantification of retinal IS/OS damage in en-face OCT image,” Comput. Biol. Med. 69, 52–60 (2016).
[PubMed]

W. Zhu, H. Chen, H. Zhao, B. Tian, L. Wang, F. Shi, D. Xiang, X. Luo, E. Gao, L. Zhang, Y. Yin, and X. Chen, “Automatic Three-dimensional Detection of Photoreceptor Ellipsoid Zone Disruption Caused by Trauma in the OCT,” Sci. Rep. 6, 25433 (2016).
[PubMed]

Y. Itoh, A. Vasanji, and J. P. Ehlers, “Volumetric ellipsoid zone mapping for enhanced visualisation of outer retinal integrity with optical coherence tomography,” Br. J. Ophthalmol. 100(3), 295–299 (2016).
[PubMed]

L. W. Tao, Z. Wu, R. H. Guymer, and C. D. Luu, “Ellipsoid zone on optical coherence tomography: a review,” Clin. Experiment. Ophthalmol. 44(5), 422–430 (2016).
[PubMed]

S. S. Gao, Y. Jia, M. Zhang, J. P. Su, G. Liu, T. S. Hwang, S. T. Bailey, and D. Huang, “Optical coherence tomography angiography,” Investigative Ophthalmol. Vis. Sci. 57, OCT27–OCT36 (2016).
[PubMed]

T. S. Hwang, M. Zhang, K. Bhavsar, X. Zhang, J. P. Campbell, P. Lin, S. T. Bailey, C. J. Flaxel, A. K. Lauer, D. J. Wilson, D. Huang, and Y. Jia, “Visualization of 3 distinct retinal plexuses by projection-resolved optical coherence tomography angiography in diabetic retinopathy,” JAMA Ophthalmol. 134(12), 1411–1419 (2016).
[PubMed]

S. S. Gao, L. Liu, S. T. Bailey, C. J. Flaxel, D. Huang, D. Li, and Y. Jia, “Quantification of choroidal neovascularization vessel length using optical coherence tomography angiography,” J. Biomed. Opt. 21(7), 076010 (2016).
[PubMed]

2015 (5)

2014 (7)

B. Wolff, C. Basdekidou, V. Vasseur, J.-A. Sahel, A. Gaudric, and M. Mauget-Faÿsse, ““En face” optical coherence tomography imaging in type 2 idiopathic macular telangiectasia,” Retina 34(10), 2072–2078 (2014).
[PubMed]

A. Rodriguez and A. Laio, “Clustering by fast search and find of density peaks,” Science 344(6191), 1492–1496 (2014).
[PubMed]

A. Uji, T. Murakami, N. Unoki, K. Ogino, T. Horii, S. Yoshitake, Y. Dodo, and N. Yoshimura, “Parallelism for quantitative image analysis of photoreceptor-retinal pigment epithelium complex alterations in diabetic macular edema,” Invest. Ophthalmol. Vis. Sci. 55(5), 3361–3367 (2014).
[PubMed]

S. Saxena, K. Srivastav, C. M. Cheung, J. Y. W. Ng, and T. Y. Y. Lai, “Photoreceptor inner segment ellipsoid band integrity on spectral domain optical coherence tomography,” Clin. Ophthalmol. 8, 2507–2522 (2014).
[PubMed]

Y. Jia, E. Wei, X. Wang, X. Zhang, J. C. Morrison, M. Parikh, L. H. Lombardi, D. M. Gattey, R. L. Armour, B. Edmunds, M. F. Kraus, J. G. Fujimoto, and D. Huang, “Optical Coherence Tomography Angiography of Optic Disc Perfusion in Glaucoma,” Ophthalmology 121(7), 1322–1332 (2014).
[PubMed]

G. Staurenghi, S. Sadda, U. Chakravarthy, R. F. Spaide, and International Nomenclature for Optical Coherence Tomography (IN•OCT) Panel, “Proposed Lexicon for Anatomic Landmarks in Normal Posterior Segment Spectral-Domain Optical Coherence Tomography: the IN•OCT consensus,” Ophthalmology 121(8), 1572–1578 (2014).
[PubMed]

S. Saxena, K. Srivastav, C. M. Cheung, J. Y. Ng, and T. Y. Lai, “Photoreceptor inner segment ellipsoid band integrity on spectral domain optical coherence tomography,” Clin. Ophthalmol. 8, 2507–2522 (2014).
[PubMed]

2013 (2)

A. Jain, S. Saxena, V. K. Khanna, R. K. Shukla, and C. H. Meyer, “Status of serum VEGF and ICAM-1 and its association with external limiting membrane and inner segment-outer segment junction disruption in type 2 diabetes mellitus,” Mol. Vis. 19, 1760–1768 (2013).
[PubMed]

M. B. Powner, M. C. Gillies, M. Zhu, K. Vevis, A. P. Hunyor, and M. Fruttiger, “Loss of Müller’s Cells and Photoreceptors in Macular Telangiectasia Type 2,” Ophthalmology 120(11), 2344–2352 (2013).
[PubMed]

2012 (7)

F. B. Sallo, T. Peto, C. Egan, U. E. K. Wolf-Schnurrbusch, T. E. Clemons, M. C. Gillies, D. Pauleikhoff, G. S. Rubin, E. Y. Chew, A. C. Bird, and MacTel Study Group, ““En face” OCT Imaging of the IS/OS Junction Line in Type 2 Idiopathic Macular Telangiectasia,” Invest. Ophthalmol. Vis. Sci. 53(10), 6145–6152 (2012).
[PubMed]

K. I. Hartmann, M. L. Gomez, D. U. Bartsch, A. K. Schuster, and W. R. Freeman, “Effect of change in drusen evolution on photoreceptor inner segment/outer segment junction,” Retina 32(8), 1492–1499 (2012).
[PubMed]

Y. Jia, J. C. Morrison, J. Tokayer, O. Tan, L. Lombardi, B. Baumann, C. D. Lu, W. Choi, J. G. Fujimoto, and D. Huang, “Quantitative OCT angiography of optic nerve head blood flow,” Biomed. Opt. Express 3(12), 3127–3137 (2012).
[PubMed]

J. W. Y. Yau, S. L. Rogers, R. Kawasaki, E. L. Lamoureux, J. W. Kowalski, T. Bek, S.-J. Chen, J. M. Dekker, A. Fletcher, J. Grauslund, S. Haffner, R. F. Hamman, M. K. Ikram, T. Kayama, B. E. K. Klein, R. Klein, S. Krishnaiah, K. Mayurasakorn, J. P. O’Hare, T. J. Orchard, M. Porta, M. Rema, M. S. Roy, T. Sharma, J. Shaw, H. Taylor, J. M. Tielsch, R. Varma, J. J. Wang, N. Wang, S. West, L. Xu, M. Yasuda, X. Zhang, P. Mitchell, T. Y. Wong, and Meta-Analysis for Eye Disease (META-EYE) Study Group, “Global Prevalence and Major Risk Factors of Diabetic Retinopathy,” Diabetes Care 35(3), 556–564 (2012).
[PubMed]

Y. Jia, O. Tan, J. Tokayer, B. Potsaid, Y. Wang, J. J. Liu, M. F. Kraus, H. Subhash, J. G. Fujimoto, J. Hornegger, and D. Huang, “Split-spectrum amplitude-decorrelation angiography with optical coherence tomography,” Opt. Express 20(4), 4710–4725 (2012).
[PubMed]

M. F. Kraus, B. Potsaid, M. A. Mayer, R. Bock, B. Baumann, J. J. Liu, J. Hornegger, and J. G. Fujimoto, “Motion correction in optical coherence tomography volumes on a per A-scan basis using orthogonal scan patterns,” Biomed. Opt. Express 3(6), 1182–1199 (2012).
[PubMed]

H. J. Shin, S. H. Lee, H. Chung, and H. C. Kim, “Association between photoreceptor integrity and visual outcome in diabetic macular edema,” Graefes Arch. Clin. Exp. Ophthalmol. 250(1), 61–70 (2012).
[PubMed]

2011 (1)

C.-W. Bong and M. Rajeswari, “Multi-objective nature-inspired clustering and classification techniques for image segmentation,” Appl. Soft Comput. 11, 3271–3282 (2011).

2010 (2)

A. S. Maheshwary, S. F. Oster, R. M. S. Yuson, L. Cheng, F. Mojana, and W. R. Freeman, “The Association Between Percent Disruption of the Photoreceptor Inner Segment-Outer Segment Junction and Visual Acuity in Diabetic Macular Edema,” Am. J. Ophthalmol. 150(1), 63–67 (2010).
[PubMed]

J. Oh, W. E. Smiddy, H. W. Flynn, G. Gregori, and B. Lujan, “Photoreceptor inner/outer segment defect imaging by spectral domain OCT and visual prognosis after macular hole surgery,” Invest. Ophthalmol. Vis. Sci. 51(3), 1651–1658 (2010).
[PubMed]

2006 (1)

B. Y. Kim, S. D. Smith, and P. K. Kaiser, “Optical Coherence Tomographic Patterns of Diabetic Macular Edema,” Am. J. Ophthalmol. 142(3), 405–412 (2006).
[PubMed]

2004 (1)

H. Sun, S. Wang, and Q. Jiang, “FCM-Based Model Selection Algorithms for Determining the Number of Clusters,” Pattern Recognit. 37, 2027–2037 (2004).

1991 (1)

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and et al.., “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[PubMed]

1984 (1)

J. C. Bezdek, R. Ehrlich, and W. Full, “FCM: The fuzzy c-means clustering algorithm,” Comput. Geosci. 10, 191–203 (1984).

1981 (1)

M. P. Windham, “Cluster validity for fuzzy clustering algorithms,” Fuzzy Sets Syst. 5, 177–185 (1981).

1965 (1)

L. A. Zadeh, “Fuzzy sets,” Inf. Control 8, 338–353 (1965).

Allingham, M. J.

Alonso-Caneiro, D.

D. M. Sampson, D. Alonso-Caneiro, A. L. Chew, T. Lamey, T. McLaren, J. De Roach, and F. K. Chen, “Enhanced Visualization of Subtle Outer Retinal Pathology by En Face Optical Coherence Tomography and Correlation with Multi-Modal Imaging,” PLoS One 11(12), e0168275 (2016).
[PubMed]

Andreanos, K.

M. G. Kanakis, K. Giannouli, K. Andreanos, D. Papaconstantinou, C. Koutsandrea, I. Ladas, I. Georgalas, P. Petrou, and A. I. Kotsolis, “Capillary nonperfusion and photoreceptor loss in branch retinal vein occlusion: Spatial Correlation and Morphologic Characteristics,” Retina 37(9), 1710–1722 (2017).
[PubMed]

Armour, R. L.

Y. Jia, E. Wei, X. Wang, X. Zhang, J. C. Morrison, M. Parikh, L. H. Lombardi, D. M. Gattey, R. L. Armour, B. Edmunds, M. F. Kraus, J. G. Fujimoto, and D. Huang, “Optical Coherence Tomography Angiography of Optic Disc Perfusion in Glaucoma,” Ophthalmology 121(7), 1322–1332 (2014).
[PubMed]

Bailey, S. T.

J. Wang, M. Zhang, T. S. Hwang, S. T. Bailey, D. Huang, D. J. Wilson, and Y. Jia, “Reflectance-based projection-resolved optical coherence tomography angiography [Invited],” Biomed. Opt. Express 8(3), 1536–1548 (2017).
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R. Zhao, A. Camino, J. Wang, A. M. Hagag, Y. Lu, S. T. Bailey, C. J. Flaxel, T. S. Hwang, D. Huang, D. Li, and Y. Jia, “Automated drusen detection in dry age-related macular degeneration by multiple-depth, en face optical coherence tomography,” Biomed. Opt. Express 8, 5049–5064 (2017).

M. Zhang, T. S. Hwang, J. P. Campbell, S. T. Bailey, D. J. Wilson, D. Huang, and Y. Jia, “Projection-resolved optical coherence tomographic angiography,” Biomed. Opt. Express 7(3), 816–828 (2016).
[PubMed]

T. S. Hwang, M. Zhang, K. Bhavsar, X. Zhang, J. P. Campbell, P. Lin, S. T. Bailey, C. J. Flaxel, A. K. Lauer, D. J. Wilson, D. Huang, and Y. Jia, “Visualization of 3 distinct retinal plexuses by projection-resolved optical coherence tomography angiography in diabetic retinopathy,” JAMA Ophthalmol. 134(12), 1411–1419 (2016).
[PubMed]

S. S. Gao, L. Liu, S. T. Bailey, C. J. Flaxel, D. Huang, D. Li, and Y. Jia, “Quantification of choroidal neovascularization vessel length using optical coherence tomography angiography,” J. Biomed. Opt. 21(7), 076010 (2016).
[PubMed]

S. S. Gao, Y. Jia, M. Zhang, J. P. Su, G. Liu, T. S. Hwang, S. T. Bailey, and D. Huang, “Optical coherence tomography angiography,” Investigative Ophthalmol. Vis. Sci. 57, OCT27–OCT36 (2016).
[PubMed]

M. Zhang, J. Wang, A. D. Pechauer, T. S. Hwang, S. S. Gao, L. Liu, L. Liu, S. T. Bailey, D. J. Wilson, D. Huang, and Y. Jia, “Advanced image processing for optical coherence tomographic angiography of macular diseases,” Biomed. Opt. Express 6(12), 4661–4675 (2015).
[PubMed]

Bartsch, D. U.

K. I. Hartmann, M. L. Gomez, D. U. Bartsch, A. K. Schuster, and W. R. Freeman, “Effect of change in drusen evolution on photoreceptor inner segment/outer segment junction,” Retina 32(8), 1492–1499 (2012).
[PubMed]

Basdekidou, C.

B. Wolff, C. Basdekidou, V. Vasseur, J.-A. Sahel, A. Gaudric, and M. Mauget-Faÿsse, ““En face” optical coherence tomography imaging in type 2 idiopathic macular telangiectasia,” Retina 34(10), 2072–2078 (2014).
[PubMed]

Baumann, B.

Bek, T.

J. W. Y. Yau, S. L. Rogers, R. Kawasaki, E. L. Lamoureux, J. W. Kowalski, T. Bek, S.-J. Chen, J. M. Dekker, A. Fletcher, J. Grauslund, S. Haffner, R. F. Hamman, M. K. Ikram, T. Kayama, B. E. K. Klein, R. Klein, S. Krishnaiah, K. Mayurasakorn, J. P. O’Hare, T. J. Orchard, M. Porta, M. Rema, M. S. Roy, T. Sharma, J. Shaw, H. Taylor, J. M. Tielsch, R. Varma, J. J. Wang, N. Wang, S. West, L. Xu, M. Yasuda, X. Zhang, P. Mitchell, T. Y. Wong, and Meta-Analysis for Eye Disease (META-EYE) Study Group, “Global Prevalence and Major Risk Factors of Diabetic Retinopathy,” Diabetes Care 35(3), 556–564 (2012).
[PubMed]

Bezdek, J. C.

J. C. Bezdek, R. Ehrlich, and W. Full, “FCM: The fuzzy c-means clustering algorithm,” Comput. Geosci. 10, 191–203 (1984).

Bhavsar, K.

T. S. Hwang, M. Zhang, K. Bhavsar, X. Zhang, J. P. Campbell, P. Lin, S. T. Bailey, C. J. Flaxel, A. K. Lauer, D. J. Wilson, D. Huang, and Y. Jia, “Visualization of 3 distinct retinal plexuses by projection-resolved optical coherence tomography angiography in diabetic retinopathy,” JAMA Ophthalmol. 134(12), 1411–1419 (2016).
[PubMed]

Bird, A. C.

F. B. Sallo, T. Peto, C. Egan, U. E. K. Wolf-Schnurrbusch, T. E. Clemons, M. C. Gillies, D. Pauleikhoff, G. S. Rubin, E. Y. Chew, A. C. Bird, and MacTel Study Group, ““En face” OCT Imaging of the IS/OS Junction Line in Type 2 Idiopathic Macular Telangiectasia,” Invest. Ophthalmol. Vis. Sci. 53(10), 6145–6152 (2012).
[PubMed]

Bock, R.

Bogunovic, H.

Bong, C.-W.

C.-W. Bong and M. Rajeswari, “Multi-objective nature-inspired clustering and classification techniques for image segmentation,” Appl. Soft Comput. 11, 3271–3282 (2011).

Camino, A.

Campbell, J. P.

M. Zhang, T. S. Hwang, J. P. Campbell, S. T. Bailey, D. J. Wilson, D. Huang, and Y. Jia, “Projection-resolved optical coherence tomographic angiography,” Biomed. Opt. Express 7(3), 816–828 (2016).
[PubMed]

T. S. Hwang, M. Zhang, K. Bhavsar, X. Zhang, J. P. Campbell, P. Lin, S. T. Bailey, C. J. Flaxel, A. K. Lauer, D. J. Wilson, D. Huang, and Y. Jia, “Visualization of 3 distinct retinal plexuses by projection-resolved optical coherence tomography angiography in diabetic retinopathy,” JAMA Ophthalmol. 134(12), 1411–1419 (2016).
[PubMed]

Carroll, J.

L. W. Sun, J. Carroll, and B. J. Lujan, “Photoreceptor disruption and vision loss associated with central serous retinopathy,” American Journal of Ophthalmology Case Reports 8, 74–77 (2017).

Chakravarthy, U.

G. Staurenghi, S. Sadda, U. Chakravarthy, R. F. Spaide, and International Nomenclature for Optical Coherence Tomography (IN•OCT) Panel, “Proposed Lexicon for Anatomic Landmarks in Normal Posterior Segment Spectral-Domain Optical Coherence Tomography: the IN•OCT consensus,” Ophthalmology 121(8), 1572–1578 (2014).
[PubMed]

Chang, W.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and et al.., “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[PubMed]

Chen, F. K.

D. M. Sampson, D. Alonso-Caneiro, A. L. Chew, T. Lamey, T. McLaren, J. De Roach, and F. K. Chen, “Enhanced Visualization of Subtle Outer Retinal Pathology by En Face Optical Coherence Tomography and Correlation with Multi-Modal Imaging,” PLoS One 11(12), e0168275 (2016).
[PubMed]

Chen, H.

W. Zhu, H. Chen, H. Zhao, B. Tian, L. Wang, F. Shi, D. Xiang, X. Luo, E. Gao, L. Zhang, Y. Yin, and X. Chen, “Automatic Three-dimensional Detection of Photoreceptor Ellipsoid Zone Disruption Caused by Trauma in the OCT,” Sci. Rep. 6, 25433 (2016).
[PubMed]

Chen, Q.

Q. Chen, S. Huang, Q. Ma, H. Lin, M. Pan, X. Liu, F. Lu, and M. Shen, “Ultra-high resolution profiles of macular intra-retinal layer thicknesses and associations with visual field defects in primary open angle glaucoma,” Sci. Rep. 7, 41100 (2017).
[PubMed]

Chen, S.-J.

J. W. Y. Yau, S. L. Rogers, R. Kawasaki, E. L. Lamoureux, J. W. Kowalski, T. Bek, S.-J. Chen, J. M. Dekker, A. Fletcher, J. Grauslund, S. Haffner, R. F. Hamman, M. K. Ikram, T. Kayama, B. E. K. Klein, R. Klein, S. Krishnaiah, K. Mayurasakorn, J. P. O’Hare, T. J. Orchard, M. Porta, M. Rema, M. S. Roy, T. Sharma, J. Shaw, H. Taylor, J. M. Tielsch, R. Varma, J. J. Wang, N. Wang, S. West, L. Xu, M. Yasuda, X. Zhang, P. Mitchell, T. Y. Wong, and Meta-Analysis for Eye Disease (META-EYE) Study Group, “Global Prevalence and Major Risk Factors of Diabetic Retinopathy,” Diabetes Care 35(3), 556–564 (2012).
[PubMed]

Chen, X.

W. Zhu, H. Chen, H. Zhao, B. Tian, L. Wang, F. Shi, D. Xiang, X. Luo, E. Gao, L. Zhang, Y. Yin, and X. Chen, “Automatic Three-dimensional Detection of Photoreceptor Ellipsoid Zone Disruption Caused by Trauma in the OCT,” Sci. Rep. 6, 25433 (2016).
[PubMed]

Cheng, L.

A. S. Maheshwary, S. F. Oster, R. M. S. Yuson, L. Cheng, F. Mojana, and W. R. Freeman, “The Association Between Percent Disruption of the Photoreceptor Inner Segment-Outer Segment Junction and Visual Acuity in Diabetic Macular Edema,” Am. J. Ophthalmol. 150(1), 63–67 (2010).
[PubMed]

Cheung, C. M.

S. Saxena, K. Srivastav, C. M. Cheung, J. Y. W. Ng, and T. Y. Y. Lai, “Photoreceptor inner segment ellipsoid band integrity on spectral domain optical coherence tomography,” Clin. Ophthalmol. 8, 2507–2522 (2014).
[PubMed]

S. Saxena, K. Srivastav, C. M. Cheung, J. Y. Ng, and T. Y. Lai, “Photoreceptor inner segment ellipsoid band integrity on spectral domain optical coherence tomography,” Clin. Ophthalmol. 8, 2507–2522 (2014).
[PubMed]

Chew, A. L.

D. M. Sampson, D. Alonso-Caneiro, A. L. Chew, T. Lamey, T. McLaren, J. De Roach, and F. K. Chen, “Enhanced Visualization of Subtle Outer Retinal Pathology by En Face Optical Coherence Tomography and Correlation with Multi-Modal Imaging,” PLoS One 11(12), e0168275 (2016).
[PubMed]

Chew, E. Y.

D. Mukherjee, E. M. Lad, R. R. Vann, S. J. Jaffe, T. E. Clemons, M. Friedlander, E. Y. Chew, G. J. Jaffe, S. Farsiu, and MacTel Study Group, “Correlation Between Macular Integrity Assessment and Optical Coherence Tomography Imaging of Ellipsoid Zone in Macular Telangiectasia Type 2,” Invest. Ophthalmol. Vis. Sci. 58(6), BIO291 (2017).
[PubMed]

F. B. Sallo, T. Peto, C. Egan, U. E. K. Wolf-Schnurrbusch, T. E. Clemons, M. C. Gillies, D. Pauleikhoff, G. S. Rubin, E. Y. Chew, A. C. Bird, and MacTel Study Group, ““En face” OCT Imaging of the IS/OS Junction Line in Type 2 Idiopathic Macular Telangiectasia,” Invest. Ophthalmol. Vis. Sci. 53(10), 6145–6152 (2012).
[PubMed]

Chhablani, J.

V. S. Gattani, K. K. Vupparaboina, A. Patil, J. Chhablani, A. Richhariya, and S. Jana, “Semi-automated quantification of retinal IS/OS damage in en-face OCT image,” Comput. Biol. Med. 69, 52–60 (2016).
[PubMed]

Chiu, S. J.

Choi, W.

Chung, H.

H. J. Shin, S. H. Lee, H. Chung, and H. C. Kim, “Association between photoreceptor integrity and visual outcome in diabetic macular edema,” Graefes Arch. Clin. Exp. Ophthalmol. 250(1), 61–70 (2012).
[PubMed]

Clemons, T. E.

D. Mukherjee, E. M. Lad, R. R. Vann, S. J. Jaffe, T. E. Clemons, M. Friedlander, E. Y. Chew, G. J. Jaffe, S. Farsiu, and MacTel Study Group, “Correlation Between Macular Integrity Assessment and Optical Coherence Tomography Imaging of Ellipsoid Zone in Macular Telangiectasia Type 2,” Invest. Ophthalmol. Vis. Sci. 58(6), BIO291 (2017).
[PubMed]

F. B. Sallo, T. Peto, C. Egan, U. E. K. Wolf-Schnurrbusch, T. E. Clemons, M. C. Gillies, D. Pauleikhoff, G. S. Rubin, E. Y. Chew, A. C. Bird, and MacTel Study Group, ““En face” OCT Imaging of the IS/OS Junction Line in Type 2 Idiopathic Macular Telangiectasia,” Invest. Ophthalmol. Vis. Sci. 53(10), 6145–6152 (2012).
[PubMed]

Cousins, S. W.

Cunefare, D.

De Roach, J.

D. M. Sampson, D. Alonso-Caneiro, A. L. Chew, T. Lamey, T. McLaren, J. De Roach, and F. K. Chen, “Enhanced Visualization of Subtle Outer Retinal Pathology by En Face Optical Coherence Tomography and Correlation with Multi-Modal Imaging,” PLoS One 11(12), e0168275 (2016).
[PubMed]

Dekker, J. M.

J. W. Y. Yau, S. L. Rogers, R. Kawasaki, E. L. Lamoureux, J. W. Kowalski, T. Bek, S.-J. Chen, J. M. Dekker, A. Fletcher, J. Grauslund, S. Haffner, R. F. Hamman, M. K. Ikram, T. Kayama, B. E. K. Klein, R. Klein, S. Krishnaiah, K. Mayurasakorn, J. P. O’Hare, T. J. Orchard, M. Porta, M. Rema, M. S. Roy, T. Sharma, J. Shaw, H. Taylor, J. M. Tielsch, R. Varma, J. J. Wang, N. Wang, S. West, L. Xu, M. Yasuda, X. Zhang, P. Mitchell, T. Y. Wong, and Meta-Analysis for Eye Disease (META-EYE) Study Group, “Global Prevalence and Major Risk Factors of Diabetic Retinopathy,” Diabetes Care 35(3), 556–564 (2012).
[PubMed]

Dodo, Y.

A. Uji, T. Murakami, N. Unoki, K. Ogino, T. Horii, S. Yoshitake, Y. Dodo, and N. Yoshimura, “Parallelism for quantitative image analysis of photoreceptor-retinal pigment epithelium complex alterations in diabetic macular edema,” Invest. Ophthalmol. Vis. Sci. 55(5), 3361–3367 (2014).
[PubMed]

Edmunds, B.

Y. Jia, E. Wei, X. Wang, X. Zhang, J. C. Morrison, M. Parikh, L. H. Lombardi, D. M. Gattey, R. L. Armour, B. Edmunds, M. F. Kraus, J. G. Fujimoto, and D. Huang, “Optical Coherence Tomography Angiography of Optic Disc Perfusion in Glaucoma,” Ophthalmology 121(7), 1322–1332 (2014).
[PubMed]

Egan, C.

F. B. Sallo, T. Peto, C. Egan, U. E. K. Wolf-Schnurrbusch, T. E. Clemons, M. C. Gillies, D. Pauleikhoff, G. S. Rubin, E. Y. Chew, A. C. Bird, and MacTel Study Group, ““En face” OCT Imaging of the IS/OS Junction Line in Type 2 Idiopathic Macular Telangiectasia,” Invest. Ophthalmol. Vis. Sci. 53(10), 6145–6152 (2012).
[PubMed]

Ehlers, J. P.

A. P. Runkle, P. K. Kaiser, S. K. Srivastava, A. P. Schachat, J. L. Reese, and J. P. Ehlers, “OCT Angiography and Ellipsoid Zone Mapping of Macular Telangiectasia Type 2 From the AVATAR Study,” Invest. Ophthalmol. Vis. Sci. 58(9), 3683–3689 (2017).
[PubMed]

Y. Itoh, A. Vasanji, and J. P. Ehlers, “Volumetric ellipsoid zone mapping for enhanced visualisation of outer retinal integrity with optical coherence tomography,” Br. J. Ophthalmol. 100(3), 295–299 (2016).
[PubMed]

Ehrlich, R.

J. C. Bezdek, R. Ehrlich, and W. Full, “FCM: The fuzzy c-means clustering algorithm,” Comput. Geosci. 10, 191–203 (1984).

Fang, L.

Farsiu, S.

Flaxel, C. J.

R. Zhao, A. Camino, J. Wang, A. M. Hagag, Y. Lu, S. T. Bailey, C. J. Flaxel, T. S. Hwang, D. Huang, D. Li, and Y. Jia, “Automated drusen detection in dry age-related macular degeneration by multiple-depth, en face optical coherence tomography,” Biomed. Opt. Express 8, 5049–5064 (2017).

P. Zang, S. S. Gao, T. S. Hwang, C. J. Flaxel, D. J. Wilson, J. C. Morrison, D. Huang, D. Li, and Y. Jia, “Automated boundary detection of the optic disc and layer segmentation of the peripapillary retina in volumetric structural and angiographic optical coherence tomography,” Biomed. Opt. Express 8(3), 1306–1318 (2017).
[PubMed]

S. S. Gao, L. Liu, S. T. Bailey, C. J. Flaxel, D. Huang, D. Li, and Y. Jia, “Quantification of choroidal neovascularization vessel length using optical coherence tomography angiography,” J. Biomed. Opt. 21(7), 076010 (2016).
[PubMed]

T. S. Hwang, M. Zhang, K. Bhavsar, X. Zhang, J. P. Campbell, P. Lin, S. T. Bailey, C. J. Flaxel, A. K. Lauer, D. J. Wilson, D. Huang, and Y. Jia, “Visualization of 3 distinct retinal plexuses by projection-resolved optical coherence tomography angiography in diabetic retinopathy,” JAMA Ophthalmol. 134(12), 1411–1419 (2016).
[PubMed]

Fletcher, A.

J. W. Y. Yau, S. L. Rogers, R. Kawasaki, E. L. Lamoureux, J. W. Kowalski, T. Bek, S.-J. Chen, J. M. Dekker, A. Fletcher, J. Grauslund, S. Haffner, R. F. Hamman, M. K. Ikram, T. Kayama, B. E. K. Klein, R. Klein, S. Krishnaiah, K. Mayurasakorn, J. P. O’Hare, T. J. Orchard, M. Porta, M. Rema, M. S. Roy, T. Sharma, J. Shaw, H. Taylor, J. M. Tielsch, R. Varma, J. J. Wang, N. Wang, S. West, L. Xu, M. Yasuda, X. Zhang, P. Mitchell, T. Y. Wong, and Meta-Analysis for Eye Disease (META-EYE) Study Group, “Global Prevalence and Major Risk Factors of Diabetic Retinopathy,” Diabetes Care 35(3), 556–564 (2012).
[PubMed]

Flotte, T.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and et al.., “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[PubMed]

Flynn, H. W.

J. Oh, W. E. Smiddy, H. W. Flynn, G. Gregori, and B. Lujan, “Photoreceptor inner/outer segment defect imaging by spectral domain OCT and visual prognosis after macular hole surgery,” Invest. Ophthalmol. Vis. Sci. 51(3), 1651–1658 (2010).
[PubMed]

Francis, A. W.

A. W. Francis, J. Wanek, J. I. Lim, and M. Shahidi, “Enface Thickness Mapping and Reflectance Imaging of Retinal Layers in Diabetic Retinopathy,” PLoS One 10(12), e0145628 (2015).
[PubMed]

Freeman, W. R.

K. I. Hartmann, M. L. Gomez, D. U. Bartsch, A. K. Schuster, and W. R. Freeman, “Effect of change in drusen evolution on photoreceptor inner segment/outer segment junction,” Retina 32(8), 1492–1499 (2012).
[PubMed]

A. S. Maheshwary, S. F. Oster, R. M. S. Yuson, L. Cheng, F. Mojana, and W. R. Freeman, “The Association Between Percent Disruption of the Photoreceptor Inner Segment-Outer Segment Junction and Visual Acuity in Diabetic Macular Edema,” Am. J. Ophthalmol. 150(1), 63–67 (2010).
[PubMed]

Friedlander, M.

D. Mukherjee, E. M. Lad, R. R. Vann, S. J. Jaffe, T. E. Clemons, M. Friedlander, E. Y. Chew, G. J. Jaffe, S. Farsiu, and MacTel Study Group, “Correlation Between Macular Integrity Assessment and Optical Coherence Tomography Imaging of Ellipsoid Zone in Macular Telangiectasia Type 2,” Invest. Ophthalmol. Vis. Sci. 58(6), BIO291 (2017).
[PubMed]

Fruttiger, M.

M. B. Powner, M. C. Gillies, M. Zhu, K. Vevis, A. P. Hunyor, and M. Fruttiger, “Loss of Müller’s Cells and Photoreceptors in Macular Telangiectasia Type 2,” Ophthalmology 120(11), 2344–2352 (2013).
[PubMed]

Fujimoto, J. G.

Full, W.

J. C. Bezdek, R. Ehrlich, and W. Full, “FCM: The fuzzy c-means clustering algorithm,” Comput. Geosci. 10, 191–203 (1984).

Gao, E.

W. Zhu, H. Chen, H. Zhao, B. Tian, L. Wang, F. Shi, D. Xiang, X. Luo, E. Gao, L. Zhang, Y. Yin, and X. Chen, “Automatic Three-dimensional Detection of Photoreceptor Ellipsoid Zone Disruption Caused by Trauma in the OCT,” Sci. Rep. 6, 25433 (2016).
[PubMed]

Gao, S. S.

Gattani, V. S.

V. S. Gattani, K. K. Vupparaboina, A. Patil, J. Chhablani, A. Richhariya, and S. Jana, “Semi-automated quantification of retinal IS/OS damage in en-face OCT image,” Comput. Biol. Med. 69, 52–60 (2016).
[PubMed]

Gattey, D. M.

Y. Jia, E. Wei, X. Wang, X. Zhang, J. C. Morrison, M. Parikh, L. H. Lombardi, D. M. Gattey, R. L. Armour, B. Edmunds, M. F. Kraus, J. G. Fujimoto, and D. Huang, “Optical Coherence Tomography Angiography of Optic Disc Perfusion in Glaucoma,” Ophthalmology 121(7), 1322–1332 (2014).
[PubMed]

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B. Wolff, C. Basdekidou, V. Vasseur, J.-A. Sahel, A. Gaudric, and M. Mauget-Faÿsse, ““En face” optical coherence tomography imaging in type 2 idiopathic macular telangiectasia,” Retina 34(10), 2072–2078 (2014).
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Georgalas, I.

M. G. Kanakis, K. Giannouli, K. Andreanos, D. Papaconstantinou, C. Koutsandrea, I. Ladas, I. Georgalas, P. Petrou, and A. I. Kotsolis, “Capillary nonperfusion and photoreceptor loss in branch retinal vein occlusion: Spatial Correlation and Morphologic Characteristics,” Retina 37(9), 1710–1722 (2017).
[PubMed]

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Giannouli, K.

M. G. Kanakis, K. Giannouli, K. Andreanos, D. Papaconstantinou, C. Koutsandrea, I. Ladas, I. Georgalas, P. Petrou, and A. I. Kotsolis, “Capillary nonperfusion and photoreceptor loss in branch retinal vein occlusion: Spatial Correlation and Morphologic Characteristics,” Retina 37(9), 1710–1722 (2017).
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Gillies, M. C.

M. B. Powner, M. C. Gillies, M. Zhu, K. Vevis, A. P. Hunyor, and M. Fruttiger, “Loss of Müller’s Cells and Photoreceptors in Macular Telangiectasia Type 2,” Ophthalmology 120(11), 2344–2352 (2013).
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K. I. Hartmann, M. L. Gomez, D. U. Bartsch, A. K. Schuster, and W. R. Freeman, “Effect of change in drusen evolution on photoreceptor inner segment/outer segment junction,” Retina 32(8), 1492–1499 (2012).
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Grauslund, J.

J. W. Y. Yau, S. L. Rogers, R. Kawasaki, E. L. Lamoureux, J. W. Kowalski, T. Bek, S.-J. Chen, J. M. Dekker, A. Fletcher, J. Grauslund, S. Haffner, R. F. Hamman, M. K. Ikram, T. Kayama, B. E. K. Klein, R. Klein, S. Krishnaiah, K. Mayurasakorn, J. P. O’Hare, T. J. Orchard, M. Porta, M. Rema, M. S. Roy, T. Sharma, J. Shaw, H. Taylor, J. M. Tielsch, R. Varma, J. J. Wang, N. Wang, S. West, L. Xu, M. Yasuda, X. Zhang, P. Mitchell, T. Y. Wong, and Meta-Analysis for Eye Disease (META-EYE) Study Group, “Global Prevalence and Major Risk Factors of Diabetic Retinopathy,” Diabetes Care 35(3), 556–564 (2012).
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J. Oh, W. E. Smiddy, H. W. Flynn, G. Gregori, and B. Lujan, “Photoreceptor inner/outer segment defect imaging by spectral domain OCT and visual prognosis after macular hole surgery,” Invest. Ophthalmol. Vis. Sci. 51(3), 1651–1658 (2010).
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D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and et al.., “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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Haffner, S.

J. W. Y. Yau, S. L. Rogers, R. Kawasaki, E. L. Lamoureux, J. W. Kowalski, T. Bek, S.-J. Chen, J. M. Dekker, A. Fletcher, J. Grauslund, S. Haffner, R. F. Hamman, M. K. Ikram, T. Kayama, B. E. K. Klein, R. Klein, S. Krishnaiah, K. Mayurasakorn, J. P. O’Hare, T. J. Orchard, M. Porta, M. Rema, M. S. Roy, T. Sharma, J. Shaw, H. Taylor, J. M. Tielsch, R. Varma, J. J. Wang, N. Wang, S. West, L. Xu, M. Yasuda, X. Zhang, P. Mitchell, T. Y. Wong, and Meta-Analysis for Eye Disease (META-EYE) Study Group, “Global Prevalence and Major Risk Factors of Diabetic Retinopathy,” Diabetes Care 35(3), 556–564 (2012).
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Hagag, A. M.

Hamman, R. F.

J. W. Y. Yau, S. L. Rogers, R. Kawasaki, E. L. Lamoureux, J. W. Kowalski, T. Bek, S.-J. Chen, J. M. Dekker, A. Fletcher, J. Grauslund, S. Haffner, R. F. Hamman, M. K. Ikram, T. Kayama, B. E. K. Klein, R. Klein, S. Krishnaiah, K. Mayurasakorn, J. P. O’Hare, T. J. Orchard, M. Porta, M. Rema, M. S. Roy, T. Sharma, J. Shaw, H. Taylor, J. M. Tielsch, R. Varma, J. J. Wang, N. Wang, S. West, L. Xu, M. Yasuda, X. Zhang, P. Mitchell, T. Y. Wong, and Meta-Analysis for Eye Disease (META-EYE) Study Group, “Global Prevalence and Major Risk Factors of Diabetic Retinopathy,” Diabetes Care 35(3), 556–564 (2012).
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K. I. Hartmann, M. L. Gomez, D. U. Bartsch, A. K. Schuster, and W. R. Freeman, “Effect of change in drusen evolution on photoreceptor inner segment/outer segment junction,” Retina 32(8), 1492–1499 (2012).
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Hee, M. R.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and et al.., “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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A. Uji, T. Murakami, N. Unoki, K. Ogino, T. Horii, S. Yoshitake, Y. Dodo, and N. Yoshimura, “Parallelism for quantitative image analysis of photoreceptor-retinal pigment epithelium complex alterations in diabetic macular edema,” Invest. Ophthalmol. Vis. Sci. 55(5), 3361–3367 (2014).
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Hornegger, J.

Huang, D.

R. Zhao, A. Camino, J. Wang, A. M. Hagag, Y. Lu, S. T. Bailey, C. J. Flaxel, T. S. Hwang, D. Huang, D. Li, and Y. Jia, “Automated drusen detection in dry age-related macular degeneration by multiple-depth, en face optical coherence tomography,” Biomed. Opt. Express 8, 5049–5064 (2017).

P. Zang, S. S. Gao, T. S. Hwang, C. J. Flaxel, D. J. Wilson, J. C. Morrison, D. Huang, D. Li, and Y. Jia, “Automated boundary detection of the optic disc and layer segmentation of the peripapillary retina in volumetric structural and angiographic optical coherence tomography,” Biomed. Opt. Express 8(3), 1306–1318 (2017).
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J. Wang, M. Zhang, T. S. Hwang, S. T. Bailey, D. Huang, D. J. Wilson, and Y. Jia, “Reflectance-based projection-resolved optical coherence tomography angiography [Invited],” Biomed. Opt. Express 8(3), 1536–1548 (2017).
[PubMed]

M. Zhang, T. S. Hwang, J. P. Campbell, S. T. Bailey, D. J. Wilson, D. Huang, and Y. Jia, “Projection-resolved optical coherence tomographic angiography,” Biomed. Opt. Express 7(3), 816–828 (2016).
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S. S. Gao, Y. Jia, M. Zhang, J. P. Su, G. Liu, T. S. Hwang, S. T. Bailey, and D. Huang, “Optical coherence tomography angiography,” Investigative Ophthalmol. Vis. Sci. 57, OCT27–OCT36 (2016).
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S. S. Gao, L. Liu, S. T. Bailey, C. J. Flaxel, D. Huang, D. Li, and Y. Jia, “Quantification of choroidal neovascularization vessel length using optical coherence tomography angiography,” J. Biomed. Opt. 21(7), 076010 (2016).
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T. S. Hwang, M. Zhang, K. Bhavsar, X. Zhang, J. P. Campbell, P. Lin, S. T. Bailey, C. J. Flaxel, A. K. Lauer, D. J. Wilson, D. Huang, and Y. Jia, “Visualization of 3 distinct retinal plexuses by projection-resolved optical coherence tomography angiography in diabetic retinopathy,” JAMA Ophthalmol. 134(12), 1411–1419 (2016).
[PubMed]

S. S. Gao, G. Liu, D. Huang, and Y. Jia, “Optimization of the split-spectrum amplitude-decorrelation angiography algorithm on a spectral optical coherence tomography system,” Opt. Lett. 40(10), 2305–2308 (2015).
[PubMed]

M. Zhang, J. Wang, A. D. Pechauer, T. S. Hwang, S. S. Gao, L. Liu, L. Liu, S. T. Bailey, D. J. Wilson, D. Huang, and Y. Jia, “Advanced image processing for optical coherence tomographic angiography of macular diseases,” Biomed. Opt. Express 6(12), 4661–4675 (2015).
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Y. Jia, E. Wei, X. Wang, X. Zhang, J. C. Morrison, M. Parikh, L. H. Lombardi, D. M. Gattey, R. L. Armour, B. Edmunds, M. F. Kraus, J. G. Fujimoto, and D. Huang, “Optical Coherence Tomography Angiography of Optic Disc Perfusion in Glaucoma,” Ophthalmology 121(7), 1322–1332 (2014).
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Y. Jia, O. Tan, J. Tokayer, B. Potsaid, Y. Wang, J. J. Liu, M. F. Kraus, H. Subhash, J. G. Fujimoto, J. Hornegger, and D. Huang, “Split-spectrum amplitude-decorrelation angiography with optical coherence tomography,” Opt. Express 20(4), 4710–4725 (2012).
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Y. Jia, J. C. Morrison, J. Tokayer, O. Tan, L. Lombardi, B. Baumann, C. D. Lu, W. Choi, J. G. Fujimoto, and D. Huang, “Quantitative OCT angiography of optic nerve head blood flow,” Biomed. Opt. Express 3(12), 3127–3137 (2012).
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D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and et al.., “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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Huang, S.

Q. Chen, S. Huang, Q. Ma, H. Lin, M. Pan, X. Liu, F. Lu, and M. Shen, “Ultra-high resolution profiles of macular intra-retinal layer thicknesses and associations with visual field defects in primary open angle glaucoma,” Sci. Rep. 7, 41100 (2017).
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Hunyor, A. P.

M. B. Powner, M. C. Gillies, M. Zhu, K. Vevis, A. P. Hunyor, and M. Fruttiger, “Loss of Müller’s Cells and Photoreceptors in Macular Telangiectasia Type 2,” Ophthalmology 120(11), 2344–2352 (2013).
[PubMed]

Hwang, T. S.

P. Zang, S. S. Gao, T. S. Hwang, C. J. Flaxel, D. J. Wilson, J. C. Morrison, D. Huang, D. Li, and Y. Jia, “Automated boundary detection of the optic disc and layer segmentation of the peripapillary retina in volumetric structural and angiographic optical coherence tomography,” Biomed. Opt. Express 8(3), 1306–1318 (2017).
[PubMed]

J. Wang, M. Zhang, T. S. Hwang, S. T. Bailey, D. Huang, D. J. Wilson, and Y. Jia, “Reflectance-based projection-resolved optical coherence tomography angiography [Invited],” Biomed. Opt. Express 8(3), 1536–1548 (2017).
[PubMed]

R. Zhao, A. Camino, J. Wang, A. M. Hagag, Y. Lu, S. T. Bailey, C. J. Flaxel, T. S. Hwang, D. Huang, D. Li, and Y. Jia, “Automated drusen detection in dry age-related macular degeneration by multiple-depth, en face optical coherence tomography,” Biomed. Opt. Express 8, 5049–5064 (2017).

M. Zhang, T. S. Hwang, J. P. Campbell, S. T. Bailey, D. J. Wilson, D. Huang, and Y. Jia, “Projection-resolved optical coherence tomographic angiography,” Biomed. Opt. Express 7(3), 816–828 (2016).
[PubMed]

T. S. Hwang, M. Zhang, K. Bhavsar, X. Zhang, J. P. Campbell, P. Lin, S. T. Bailey, C. J. Flaxel, A. K. Lauer, D. J. Wilson, D. Huang, and Y. Jia, “Visualization of 3 distinct retinal plexuses by projection-resolved optical coherence tomography angiography in diabetic retinopathy,” JAMA Ophthalmol. 134(12), 1411–1419 (2016).
[PubMed]

S. S. Gao, Y. Jia, M. Zhang, J. P. Su, G. Liu, T. S. Hwang, S. T. Bailey, and D. Huang, “Optical coherence tomography angiography,” Investigative Ophthalmol. Vis. Sci. 57, OCT27–OCT36 (2016).
[PubMed]

M. Zhang, J. Wang, A. D. Pechauer, T. S. Hwang, S. S. Gao, L. Liu, L. Liu, S. T. Bailey, D. J. Wilson, D. Huang, and Y. Jia, “Advanced image processing for optical coherence tomographic angiography of macular diseases,” Biomed. Opt. Express 6(12), 4661–4675 (2015).
[PubMed]

Ikram, M. K.

J. W. Y. Yau, S. L. Rogers, R. Kawasaki, E. L. Lamoureux, J. W. Kowalski, T. Bek, S.-J. Chen, J. M. Dekker, A. Fletcher, J. Grauslund, S. Haffner, R. F. Hamman, M. K. Ikram, T. Kayama, B. E. K. Klein, R. Klein, S. Krishnaiah, K. Mayurasakorn, J. P. O’Hare, T. J. Orchard, M. Porta, M. Rema, M. S. Roy, T. Sharma, J. Shaw, H. Taylor, J. M. Tielsch, R. Varma, J. J. Wang, N. Wang, S. West, L. Xu, M. Yasuda, X. Zhang, P. Mitchell, T. Y. Wong, and Meta-Analysis for Eye Disease (META-EYE) Study Group, “Global Prevalence and Major Risk Factors of Diabetic Retinopathy,” Diabetes Care 35(3), 556–564 (2012).
[PubMed]

Itoh, Y.

Y. Itoh, A. Vasanji, and J. P. Ehlers, “Volumetric ellipsoid zone mapping for enhanced visualisation of outer retinal integrity with optical coherence tomography,” Br. J. Ophthalmol. 100(3), 295–299 (2016).
[PubMed]

Izatt, J. A.

Jaffe, G. J.

D. Mukherjee, E. M. Lad, R. R. Vann, S. J. Jaffe, T. E. Clemons, M. Friedlander, E. Y. Chew, G. J. Jaffe, S. Farsiu, and MacTel Study Group, “Correlation Between Macular Integrity Assessment and Optical Coherence Tomography Imaging of Ellipsoid Zone in Macular Telangiectasia Type 2,” Invest. Ophthalmol. Vis. Sci. 58(6), BIO291 (2017).
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Jaffe, S. J.

D. Mukherjee, E. M. Lad, R. R. Vann, S. J. Jaffe, T. E. Clemons, M. Friedlander, E. Y. Chew, G. J. Jaffe, S. Farsiu, and MacTel Study Group, “Correlation Between Macular Integrity Assessment and Optical Coherence Tomography Imaging of Ellipsoid Zone in Macular Telangiectasia Type 2,” Invest. Ophthalmol. Vis. Sci. 58(6), BIO291 (2017).
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Jain, A.

A. Jain, S. Saxena, V. K. Khanna, R. K. Shukla, and C. H. Meyer, “Status of serum VEGF and ICAM-1 and its association with external limiting membrane and inner segment-outer segment junction disruption in type 2 diabetes mellitus,” Mol. Vis. 19, 1760–1768 (2013).
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Jana, S.

V. S. Gattani, K. K. Vupparaboina, A. Patil, J. Chhablani, A. Richhariya, and S. Jana, “Semi-automated quantification of retinal IS/OS damage in en-face OCT image,” Comput. Biol. Med. 69, 52–60 (2016).
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Jia, Y.

P. Zang, S. S. Gao, T. S. Hwang, C. J. Flaxel, D. J. Wilson, J. C. Morrison, D. Huang, D. Li, and Y. Jia, “Automated boundary detection of the optic disc and layer segmentation of the peripapillary retina in volumetric structural and angiographic optical coherence tomography,” Biomed. Opt. Express 8(3), 1306–1318 (2017).
[PubMed]

J. Wang, M. Zhang, T. S. Hwang, S. T. Bailey, D. Huang, D. J. Wilson, and Y. Jia, “Reflectance-based projection-resolved optical coherence tomography angiography [Invited],” Biomed. Opt. Express 8(3), 1536–1548 (2017).
[PubMed]

R. Zhao, A. Camino, J. Wang, A. M. Hagag, Y. Lu, S. T. Bailey, C. J. Flaxel, T. S. Hwang, D. Huang, D. Li, and Y. Jia, “Automated drusen detection in dry age-related macular degeneration by multiple-depth, en face optical coherence tomography,” Biomed. Opt. Express 8, 5049–5064 (2017).

M. Zhang, T. S. Hwang, J. P. Campbell, S. T. Bailey, D. J. Wilson, D. Huang, and Y. Jia, “Projection-resolved optical coherence tomographic angiography,” Biomed. Opt. Express 7(3), 816–828 (2016).
[PubMed]

S. S. Gao, Y. Jia, M. Zhang, J. P. Su, G. Liu, T. S. Hwang, S. T. Bailey, and D. Huang, “Optical coherence tomography angiography,” Investigative Ophthalmol. Vis. Sci. 57, OCT27–OCT36 (2016).
[PubMed]

T. S. Hwang, M. Zhang, K. Bhavsar, X. Zhang, J. P. Campbell, P. Lin, S. T. Bailey, C. J. Flaxel, A. K. Lauer, D. J. Wilson, D. Huang, and Y. Jia, “Visualization of 3 distinct retinal plexuses by projection-resolved optical coherence tomography angiography in diabetic retinopathy,” JAMA Ophthalmol. 134(12), 1411–1419 (2016).
[PubMed]

S. S. Gao, L. Liu, S. T. Bailey, C. J. Flaxel, D. Huang, D. Li, and Y. Jia, “Quantification of choroidal neovascularization vessel length using optical coherence tomography angiography,” J. Biomed. Opt. 21(7), 076010 (2016).
[PubMed]

S. S. Gao, G. Liu, D. Huang, and Y. Jia, “Optimization of the split-spectrum amplitude-decorrelation angiography algorithm on a spectral optical coherence tomography system,” Opt. Lett. 40(10), 2305–2308 (2015).
[PubMed]

M. Zhang, J. Wang, A. D. Pechauer, T. S. Hwang, S. S. Gao, L. Liu, L. Liu, S. T. Bailey, D. J. Wilson, D. Huang, and Y. Jia, “Advanced image processing for optical coherence tomographic angiography of macular diseases,” Biomed. Opt. Express 6(12), 4661–4675 (2015).
[PubMed]

Y. Jia, E. Wei, X. Wang, X. Zhang, J. C. Morrison, M. Parikh, L. H. Lombardi, D. M. Gattey, R. L. Armour, B. Edmunds, M. F. Kraus, J. G. Fujimoto, and D. Huang, “Optical Coherence Tomography Angiography of Optic Disc Perfusion in Glaucoma,” Ophthalmology 121(7), 1322–1332 (2014).
[PubMed]

Y. Jia, J. C. Morrison, J. Tokayer, O. Tan, L. Lombardi, B. Baumann, C. D. Lu, W. Choi, J. G. Fujimoto, and D. Huang, “Quantitative OCT angiography of optic nerve head blood flow,” Biomed. Opt. Express 3(12), 3127–3137 (2012).
[PubMed]

Y. Jia, O. Tan, J. Tokayer, B. Potsaid, Y. Wang, J. J. Liu, M. F. Kraus, H. Subhash, J. G. Fujimoto, J. Hornegger, and D. Huang, “Split-spectrum amplitude-decorrelation angiography with optical coherence tomography,” Opt. Express 20(4), 4710–4725 (2012).
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H. Sun, S. Wang, and Q. Jiang, “FCM-Based Model Selection Algorithms for Determining the Number of Clusters,” Pattern Recognit. 37, 2027–2037 (2004).

Kaiser, P. K.

A. P. Runkle, P. K. Kaiser, S. K. Srivastava, A. P. Schachat, J. L. Reese, and J. P. Ehlers, “OCT Angiography and Ellipsoid Zone Mapping of Macular Telangiectasia Type 2 From the AVATAR Study,” Invest. Ophthalmol. Vis. Sci. 58(9), 3683–3689 (2017).
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B. Y. Kim, S. D. Smith, and P. K. Kaiser, “Optical Coherence Tomographic Patterns of Diabetic Macular Edema,” Am. J. Ophthalmol. 142(3), 405–412 (2006).
[PubMed]

Kanakis, M. G.

M. G. Kanakis, K. Giannouli, K. Andreanos, D. Papaconstantinou, C. Koutsandrea, I. Ladas, I. Georgalas, P. Petrou, and A. I. Kotsolis, “Capillary nonperfusion and photoreceptor loss in branch retinal vein occlusion: Spatial Correlation and Morphologic Characteristics,” Retina 37(9), 1710–1722 (2017).
[PubMed]

Kawasaki, R.

J. W. Y. Yau, S. L. Rogers, R. Kawasaki, E. L. Lamoureux, J. W. Kowalski, T. Bek, S.-J. Chen, J. M. Dekker, A. Fletcher, J. Grauslund, S. Haffner, R. F. Hamman, M. K. Ikram, T. Kayama, B. E. K. Klein, R. Klein, S. Krishnaiah, K. Mayurasakorn, J. P. O’Hare, T. J. Orchard, M. Porta, M. Rema, M. S. Roy, T. Sharma, J. Shaw, H. Taylor, J. M. Tielsch, R. Varma, J. J. Wang, N. Wang, S. West, L. Xu, M. Yasuda, X. Zhang, P. Mitchell, T. Y. Wong, and Meta-Analysis for Eye Disease (META-EYE) Study Group, “Global Prevalence and Major Risk Factors of Diabetic Retinopathy,” Diabetes Care 35(3), 556–564 (2012).
[PubMed]

Kayama, T.

J. W. Y. Yau, S. L. Rogers, R. Kawasaki, E. L. Lamoureux, J. W. Kowalski, T. Bek, S.-J. Chen, J. M. Dekker, A. Fletcher, J. Grauslund, S. Haffner, R. F. Hamman, M. K. Ikram, T. Kayama, B. E. K. Klein, R. Klein, S. Krishnaiah, K. Mayurasakorn, J. P. O’Hare, T. J. Orchard, M. Porta, M. Rema, M. S. Roy, T. Sharma, J. Shaw, H. Taylor, J. M. Tielsch, R. Varma, J. J. Wang, N. Wang, S. West, L. Xu, M. Yasuda, X. Zhang, P. Mitchell, T. Y. Wong, and Meta-Analysis for Eye Disease (META-EYE) Study Group, “Global Prevalence and Major Risk Factors of Diabetic Retinopathy,” Diabetes Care 35(3), 556–564 (2012).
[PubMed]

Khanna, V. K.

A. Jain, S. Saxena, V. K. Khanna, R. K. Shukla, and C. H. Meyer, “Status of serum VEGF and ICAM-1 and its association with external limiting membrane and inner segment-outer segment junction disruption in type 2 diabetes mellitus,” Mol. Vis. 19, 1760–1768 (2013).
[PubMed]

Kim, B. Y.

B. Y. Kim, S. D. Smith, and P. K. Kaiser, “Optical Coherence Tomographic Patterns of Diabetic Macular Edema,” Am. J. Ophthalmol. 142(3), 405–412 (2006).
[PubMed]

Kim, H. C.

H. J. Shin, S. H. Lee, H. Chung, and H. C. Kim, “Association between photoreceptor integrity and visual outcome in diabetic macular edema,” Graefes Arch. Clin. Exp. Ophthalmol. 250(1), 61–70 (2012).
[PubMed]

Klein, B. E. K.

J. W. Y. Yau, S. L. Rogers, R. Kawasaki, E. L. Lamoureux, J. W. Kowalski, T. Bek, S.-J. Chen, J. M. Dekker, A. Fletcher, J. Grauslund, S. Haffner, R. F. Hamman, M. K. Ikram, T. Kayama, B. E. K. Klein, R. Klein, S. Krishnaiah, K. Mayurasakorn, J. P. O’Hare, T. J. Orchard, M. Porta, M. Rema, M. S. Roy, T. Sharma, J. Shaw, H. Taylor, J. M. Tielsch, R. Varma, J. J. Wang, N. Wang, S. West, L. Xu, M. Yasuda, X. Zhang, P. Mitchell, T. Y. Wong, and Meta-Analysis for Eye Disease (META-EYE) Study Group, “Global Prevalence and Major Risk Factors of Diabetic Retinopathy,” Diabetes Care 35(3), 556–564 (2012).
[PubMed]

Klein, R.

J. W. Y. Yau, S. L. Rogers, R. Kawasaki, E. L. Lamoureux, J. W. Kowalski, T. Bek, S.-J. Chen, J. M. Dekker, A. Fletcher, J. Grauslund, S. Haffner, R. F. Hamman, M. K. Ikram, T. Kayama, B. E. K. Klein, R. Klein, S. Krishnaiah, K. Mayurasakorn, J. P. O’Hare, T. J. Orchard, M. Porta, M. Rema, M. S. Roy, T. Sharma, J. Shaw, H. Taylor, J. M. Tielsch, R. Varma, J. J. Wang, N. Wang, S. West, L. Xu, M. Yasuda, X. Zhang, P. Mitchell, T. Y. Wong, and Meta-Analysis for Eye Disease (META-EYE) Study Group, “Global Prevalence and Major Risk Factors of Diabetic Retinopathy,” Diabetes Care 35(3), 556–564 (2012).
[PubMed]

Kotsolis, A. I.

M. G. Kanakis, K. Giannouli, K. Andreanos, D. Papaconstantinou, C. Koutsandrea, I. Ladas, I. Georgalas, P. Petrou, and A. I. Kotsolis, “Capillary nonperfusion and photoreceptor loss in branch retinal vein occlusion: Spatial Correlation and Morphologic Characteristics,” Retina 37(9), 1710–1722 (2017).
[PubMed]

Koutsandrea, C.

M. G. Kanakis, K. Giannouli, K. Andreanos, D. Papaconstantinou, C. Koutsandrea, I. Ladas, I. Georgalas, P. Petrou, and A. I. Kotsolis, “Capillary nonperfusion and photoreceptor loss in branch retinal vein occlusion: Spatial Correlation and Morphologic Characteristics,” Retina 37(9), 1710–1722 (2017).
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J. W. Y. Yau, S. L. Rogers, R. Kawasaki, E. L. Lamoureux, J. W. Kowalski, T. Bek, S.-J. Chen, J. M. Dekker, A. Fletcher, J. Grauslund, S. Haffner, R. F. Hamman, M. K. Ikram, T. Kayama, B. E. K. Klein, R. Klein, S. Krishnaiah, K. Mayurasakorn, J. P. O’Hare, T. J. Orchard, M. Porta, M. Rema, M. S. Roy, T. Sharma, J. Shaw, H. Taylor, J. M. Tielsch, R. Varma, J. J. Wang, N. Wang, S. West, L. Xu, M. Yasuda, X. Zhang, P. Mitchell, T. Y. Wong, and Meta-Analysis for Eye Disease (META-EYE) Study Group, “Global Prevalence and Major Risk Factors of Diabetic Retinopathy,” Diabetes Care 35(3), 556–564 (2012).
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Figures (11)

Fig. 1
Fig. 1 Flow chart of the ellipsoid zone (EZ) defect detection algorithm. The pre-processing step generates a ratio image of registered EZ and external limiting membrane (ELM) en face images. The EZ defect detection step first stitches the ratio image under examination to a normative ratio image obtained from the healthy control group, then calculates the optimal number of clusters by a fuzzy c-means algorithm, removes noise by a median filter and finally assigns to each pixel a defect severity degree by a redefined function of membership to the defect category. The post-processing step filters out residual noise and generates the final defect severity map.
Fig. 2
Fig. 2 Routine for detection of inner boundary of ellipsoid zone (EZ) location slab. Firstly, drastic EZ segmentation changes due to large photoreceptor loss are identified by pixels with abnormally low value in an EZ/Bruch’s membrane thickness map (A). Then, the reflection of the EZ segmentation area is generated with respect to a horizontal line crossing the center of the en face image (B) and the EZ location at the pixels below threshold is substituted by the pixels in its symmetric reflection. Finally, a median filter is applied to ensure a smooth EZ segmentation across the whole scan (C). Representative B-scans are shown before (D) and after EZ smoothing (E). As observed in (D), the directional graph search algorithm can properly segment the areas with partial EZ loss but not the areas with total EZ loss.
Fig. 3
Fig. 3 Generation of external limiting membrane (ELM) and ellipsoid zone (EZ) en face images based on the smoothed EZ inner boundary segmentation . (A) A representative B-scan. The red dashed line indicates the smoothed EZ inner boundary. The blue dashed line indicates the boundary position of the slab used to generate the EZ en face image in (B). The yellow dashed line indicates the boundary position of the slab used to generate the ELM en face image in (C).
Fig. 4
Fig. 4 Illustration of the reduced signal variation on the ratio image. (A) Ellipsoid zone (EZ) en face image. (B) Ratio image. The suppression of shadowing artifacts is shown in the red boxes.
Fig. 5
Fig. 5 Different damage degree of the ellipsoid zone (EZ) observed on a ratio en face image (A) and a representative B-scan (B). The yellow arrow represents the more severely damaged EZ area; the orange arrow represent the healthy EZ area; the blue arrow represents the slightly damaged EZ area.
Fig. 6
Fig. 6 Iterating routine that calculates the optimal number of clusters to divide the en face ratio data. FCM – Fuzzy c-means.
Fig. 7
Fig. 7 Generation of a defect severity map. (A) The ratio image from a mild diabetic retinpathy scan with an ellipsoid zone (EZ) defect (upper half) is stitched to the normative ratio image obtained from a control group of ten healthy subjects (bottom half). (B) Fuzzy c-means with corrected membership function is applied on image (A) for progressively larger cluster numbers until the bottom half shows a detected area equal to zero. (C) The upper half of image (B) showing the detected EZ defect region, corrupted by peripheral noise. (D) is the defect severity map after cleanup by a median filter.
Fig. 8
Fig. 8 Comparison of the number of clusters (A) and defect area (B) found for the mild diabetic retinopathy (DR) and healthy groups upon either convergence of the iterative cluster optimization routine or reaching the maximum allowed number of iterations. Defect area is given in mm2.
Fig. 9
Fig. 9 Comparison of detection of ellipsoid zone (EZ) defect area between the automated algorithm and manual grading on B-scans in five representative diabetic retinpathy (DR) cases. The top row shows the ratio images, the middle row shows the EZ defect area extracted by the proposed algorithm. The bottom row shows the comparison of automatic detection with B-scan manual grading. The red area represents the subgroups where the EZ defect was identified correctly by both the algorithm and the grader. The light blue area represents the EZ defect subgroups detected by manual grading. The dark blue area was the healthy area detected by the manual grader. The yellow area represents the subgroups identified by the algorithm only.
Fig. 10
Fig. 10 Comparison of detection of ellipsoid zone (EZ) defect area between the automated algorithm and manual grading on ratio image. The top row shows the ratio images. The second row shows the manual grading results. Annular regions with EZ defect (red) were differentiated from regions with healthy EZ (green). The bottom row shows the EZ defect area extracted by the fuzzy logic algorithm. DR – Diabetic retinopathy.
Fig. 11
Fig. 11 Relationship between ellipsoid zone (EZ) defect area and the area with microvascular abnormalities. The top row shows the ratio images. The middle row shows the deep capillary plexus. The yellow boxes indicate areas of reduced capillary perfusion. The bottom row shows the EZ defect area extracted by the proposed algorithm. DCP – Deep capillary plexus.

Tables (2)

Tables Icon

Table 1 Performance of the proposed algorithm evaluated by manual grading of B-scans and ratio images*

Tables Icon

Table 2 Performance of the EZ loss detection algorithm based on thresholding of thickness maps generated from layer segmentation results, evaluated by manual grading of B-scans and ratio images*

Equations (5)

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R N = R μ R +2 σ R
J= i=1 K J i = i=1 K j=1 n u ij m d ij 2
c i = j=1 n u ij m R j j=1 n u ij m
u ij = 1 k=1 K ( d ij d kj ) 2 ( m1 )
M={ ( R j c 1 ) c 2 c 1 +1 }×[ R j > c 1 ]×[ R j < c 2 ]+[ R j c 1 ]

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