Abstract

As a new optical coherence tomography (OCT) imaging modality, there is no standardized quantitative interpretation of OCT angiography (OCTA) characteristics of sickle cell retinopathy (SCR). This study is to demonstrate computer-aided SCR classification using quantitative OCTA features, i.e., blood vessel tortuosity (BVT), blood vessel diameter (BVD), vessel perimeter index (VPI), foveal avascular zone (FAZ) area, FAZ contour irregularity, parafoveal avascular density (PAD). It was observed that combined features show improved classification performance, compared to single feature. Three classifiers, including support vector machine (SVM), k-nearest neighbor (KNN) algorithm, and discriminant analysis, were evaluated. Sensitivity, specificity, and accuracy were quantified to assess the performance of each classifier. For SCR vs. control classification, all three classifiers performed well with an average accuracy of 95% using the six quantitative OCTA features. For mild vs. severe stage retinopathy classification, SVM shows better (97% accuracy) performance, compared to KNN algorithm (95% accuracy) and discriminant analysis (88% accuracy).

© 2017 Optical Society of America

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2017 (3)

R. F. Spaide and C. A. Curcio, “Evaluation of Segmentation of the Superficial and Deep Vascular Layers of the Retina by Optical Coherence Tomography Angiography Instruments in Normal Eyes,” JAMA Ophthalmol. 135(3), 259–262 (2017).
[Crossref] [PubMed]

M. Alam, D. Thapa, J. I. Lim, D. Cao, and X. Yao, “Quantitative characteristics of sickle cell retinopathy in optical coherence tomography angiography,” Biomed. Opt. Express 8(3), 1741–1753 (2017).
[Crossref] [PubMed]

I. Kavakiotis, O. Tsave, A. Salifoglou, N. Maglaveras, I. Vlahavas, and I. Chouvarda, “Machine learning and data mining methods in diabetes research,” Comput. Struct. Biotechnol. J. 15, 104–116 (2017).
[Crossref] [PubMed]

2016 (5)

J. N. Kather, C.-A. Weis, F. Bianconi, S. M. Melchers, L. R. Schad, T. Gaiser, A. Marx, and F. G. Zöllner, “Multi-class texture analysis in colorectal cancer histology,” Sci. Rep. 6(1), 27988 (2016).
[Crossref] [PubMed]

Z. Chu, J. Lin, C. Gao, C. Xin, Q. Zhang, C. L. Chen, L. Roisman, G. Gregori, P. J. Rosenfeld, and R. K. Wang, “Quantitative assessment of the retinal microvasculature using optical coherence tomography angiography,” J. Biomed. Opt. 21(6), 066008 (2016).
[Crossref] [PubMed]

R. Hu and C. Ding, “Quantification of Vessel Density in Retinal Optical Coherence Tomography Angiography Images Using Local Fractal Dimension,” Invest. Ophthalmol. Vis. Sci. 57(4), 2262 (2016).
[Crossref] [PubMed]

S. G. K. Gadde, N. Anegondi, D. Bhanushali, L. Chidambara, N. K. Yadav, A. Khurana, and A. Sinha Roy, “Quantification of Vessel Density in Retinal Optical Coherence Tomography Angiography Images Using Local Fractal Dimension,” Invest. Ophthalmol. Vis. Sci. 57(1), 246–252 (2016).
[Crossref] [PubMed]

W. Minvielle, V. Caillaux, S. Y. Cohen, F. Chasset, O. Zambrowski, A. Miere, and E. H. Souied, “Macular Microangiopathy in Sickle Cell Disease Using Optical Coherence Tomography Angiography,” Am. J. Ophthalmol. 164, 137–144 (2016).
[Crossref] [PubMed]

2015 (2)

T. S. Hwang, Y. Jia, S. S. Gao, S. T. Bailey, A. K. Lauer, C. J. Flaxel, D. J. Wilson, and D. Huang, “Optical coherence tomography angiography features of diabetic retinopathy,” Retina 35(11), 2371–2376 (2015).
[Crossref] [PubMed]

Y. Jia, S. T. Bailey, T. S. Hwang, S. M. McClintic, S. S. Gao, M. E. Pennesi, C. J. Flaxel, A. K. Lauer, D. J. Wilson, J. Hornegger, J. G. Fujimoto, and D. Huang, “Quantitative optical coherence tomography angiography of vascular abnormalities in the living human eye,” Proc. Natl. Acad. Sci. U.S.A. 112(18), E2395–E2402 (2015).
[Crossref] [PubMed]

2014 (3)

B. Aliahmad, D. K. Kumar, M. G. Sarossy, and R. Jain, “Relationship between diabetes and grayscale fractal dimensions of retinal vasculature in the Indian population,” BMC Ophthalmol. 14(1), 152 (2014).
[Crossref] [PubMed]

R. Broe, M. L. Rasmussen, U. Frydkjaer-Olsen, B. S. Olsen, H. B. Mortensen, T. Peto, and J. Grauslund, “Retinal vascular fractals predict long-term microvascular complications in type 1 diabetes mellitus: the Danish Cohort of Pediatric Diabetes 1987 (DCPD1987),” Diabetologia 57(10), 2215–2221 (2014).
[Crossref] [PubMed]

E. Moult, W. Choi, N. K. Waheed, M. Adhi, B. Lee, C. D. Lu, V. Jayaraman, B. Potsaid, P. J. Rosenfeld, J. S. Duker, and J. G. Fujimoto, “Ultrahigh-speed swept-source OCT angiography in exudative AMD,” Ophthalmic Surg. Lasers Imaging Retina 45(6), 496–505 (2014).
[Crossref] [PubMed]

2013 (1)

M. T. Bonanomi and M. M. Lavezzo, “Sickle cell retinopathy: diagnosis and treatment,” Arq. Bras. Oftalmol. 76(5), 320–327 (2013).
[Crossref] [PubMed]

2012 (3)

J. I. Lim, “Ophthalmic manifestations of sickle cell disease: update of the latest findings,” Curr. Opin. Ophthalmol. 23(6), 533–536 (2012).
[Crossref] [PubMed]

S. García, J. Derrac, J. R. Cano, and F. Herrera, “Prototype selection for nearest neighbor classification: Taxonomy and empirical study,” IEEE Trans. Pattern Anal. Mach. Intell. 34(3), 417–435 (2012).
[Crossref] [PubMed]

M. Vihinen, “How to evaluate performance of prediction methods? Measures and their interpretation in variation effect analysis,” BMC Genomics 13(4Suppl 4), S2 (2012).
[Crossref] [PubMed]

2011 (2)

N. Solovieff, S. W. Hartley, C. T. Baldwin, E. S. Klings, M. T. Gladwin, J. G. Taylor, G. J. Kato, L. A. Farrer, M. H. Steinberg, and P. Sebastiani, “Ancestry of African Americans with Sickle Cell Disease,” Blood Cells Mol. Dis. 47(1), 41–45 (2011).
[Crossref] [PubMed]

Q. V. Hoang, F. Y. Chau, M. Shahidi, and J. I. Lim, “Central macular splaying and outer retinal thinning in asymptomatic sickle cell patients by spectral-domain optical coherence tomography,” Am. J. Ophthalmol. 151, 990–994 (2011).

2010 (4)

O. O. Ilesanmi, “Pathological basis of symptoms and crises in sickle cell disorder: implications for counseling and psychotherapy,” Hematol. Rep. 2(1), e2 (2010).
[Crossref] [PubMed]

A. O. Fadugbagbe, R. Q. Gurgel, C. Q. Mendonça, R. Cipolotti, A. M. dos Santos, and L. E. Cuevas, “Ocular manifestations of sickle cell disease,” Ann. Trop. Paediatr. 30(1), 19–26 (2010).
[Crossref] [PubMed]

J. W. Yau, R. Kawasaki, F. M. Islam, J. Shaw, P. Zimmet, J. J. Wang, and T. Y. Wong, “Retinal fractal dimension is increased in persons with diabetes but not impaired glucose metabolism: the Australian Diabetes, Obesity and Lifestyle (AusDiab) study,” Diabetologia 53(9), 2042–2045 (2010).
[Crossref] [PubMed]

S. Escalera, O. Pujol, and P. Radeva, “On the decoding process in ternary error-correcting output codes,” IEEE Trans. Pattern Anal. Mach. Intell. 32(1), 120–134 (2010).
[Crossref] [PubMed]

2007 (1)

2005 (1)

H. Taud and J.-F. Parrot, “Measurement of DEM roughness using the local fractal dimension,” G’eomorphologie 11(4), 327–338 (2005).
[Crossref]

2000 (1)

E. L. Allwein, R. E. Schapire, and Y. Singer, “Reducing multiclass to binary: A unifying approach for margin classifiers,” J. Mach. Learn. Res. 1, 113–141 (2000).

1999 (1)

W. E. Hart, M. Goldbaum, B. Côté, P. Kube, and M. R. Nelson, “Measurement and classification of retinal vascular tortuosity,” Int. J. Med. Inform. 53(2-3), 239–252 (1999).
[Crossref] [PubMed]

1998 (1)

T. Joachims, “Text categorization with support vector machines: Learning with many relevant features,” Mach. Learn. ECML-98, 137–142 (1998).

1978 (2)

M. H. Goldbaum, “Retinal Depression Sign Indicating a Small Retinal Infarct,” Am. J. Ophthalmol. 86(1), 45–55 (1978).
[Crossref] [PubMed]

M. H. Goldbaum, L. M. Jampol, and M. F. Goldberg, “The disc sign in sickling hemoglobinopathies,” Arch. Ophthalmol. 96(9), 1597–1600 (1978).
[Crossref] [PubMed]

1976 (1)

G. K. Asdourian, K. C. Nagpal, B. Busse, M. Goldbaum, D. Patriankos, M. F. Rabb, and M. F. Goldberg, “Macular and perimacular vascular remodelling sickling haemoglobinopathies,” Br. J. Ophthalmol. 60(6), 431–453 (1976).
[Crossref] [PubMed]

1972 (1)

P. I. Condon and G. R. Serjeant, “Ocular Findings in Homozygous Sickle Cell Anemia in Jamaica,” Am. J. Ophthalmol. 73(4), 533–543 (1972).
[Crossref] [PubMed]

1957 (1)

G. Goodman, L. Von Sallmann, and M. G. Holland, “Ocular manifestations of sickle-cell disease,” AMA Arch. Opthalmol. 58(5), 655–682 (1957).
[Crossref] [PubMed]

1954 (1)

E. W. Smith and C. L. Conley, “Clinical features of the genetic variants of sickle cell disease,” Bull. Johns Hopkins Hosp. 94(6), 289–318 (1954).
[PubMed]

Adhi, M.

E. Moult, W. Choi, N. K. Waheed, M. Adhi, B. Lee, C. D. Lu, V. Jayaraman, B. Potsaid, P. J. Rosenfeld, J. S. Duker, and J. G. Fujimoto, “Ultrahigh-speed swept-source OCT angiography in exudative AMD,” Ophthalmic Surg. Lasers Imaging Retina 45(6), 496–505 (2014).
[Crossref] [PubMed]

Alam, M.

Aliahmad, B.

B. Aliahmad, D. K. Kumar, M. G. Sarossy, and R. Jain, “Relationship between diabetes and grayscale fractal dimensions of retinal vasculature in the Indian population,” BMC Ophthalmol. 14(1), 152 (2014).
[Crossref] [PubMed]

Allwein, E. L.

E. L. Allwein, R. E. Schapire, and Y. Singer, “Reducing multiclass to binary: A unifying approach for margin classifiers,” J. Mach. Learn. Res. 1, 113–141 (2000).

Anegondi, N.

S. G. K. Gadde, N. Anegondi, D. Bhanushali, L. Chidambara, N. K. Yadav, A. Khurana, and A. Sinha Roy, “Quantification of Vessel Density in Retinal Optical Coherence Tomography Angiography Images Using Local Fractal Dimension,” Invest. Ophthalmol. Vis. Sci. 57(1), 246–252 (2016).
[Crossref] [PubMed]

Asdourian, G. K.

G. K. Asdourian, K. C. Nagpal, B. Busse, M. Goldbaum, D. Patriankos, M. F. Rabb, and M. F. Goldberg, “Macular and perimacular vascular remodelling sickling haemoglobinopathies,” Br. J. Ophthalmol. 60(6), 431–453 (1976).
[Crossref] [PubMed]

Bailey, S. T.

T. S. Hwang, Y. Jia, S. S. Gao, S. T. Bailey, A. K. Lauer, C. J. Flaxel, D. J. Wilson, and D. Huang, “Optical coherence tomography angiography features of diabetic retinopathy,” Retina 35(11), 2371–2376 (2015).
[Crossref] [PubMed]

Y. Jia, S. T. Bailey, T. S. Hwang, S. M. McClintic, S. S. Gao, M. E. Pennesi, C. J. Flaxel, A. K. Lauer, D. J. Wilson, J. Hornegger, J. G. Fujimoto, and D. Huang, “Quantitative optical coherence tomography angiography of vascular abnormalities in the living human eye,” Proc. Natl. Acad. Sci. U.S.A. 112(18), E2395–E2402 (2015).
[Crossref] [PubMed]

Baldwin, C. T.

N. Solovieff, S. W. Hartley, C. T. Baldwin, E. S. Klings, M. T. Gladwin, J. G. Taylor, G. J. Kato, L. A. Farrer, M. H. Steinberg, and P. Sebastiani, “Ancestry of African Americans with Sickle Cell Disease,” Blood Cells Mol. Dis. 47(1), 41–45 (2011).
[Crossref] [PubMed]

Bhanushali, D.

S. G. K. Gadde, N. Anegondi, D. Bhanushali, L. Chidambara, N. K. Yadav, A. Khurana, and A. Sinha Roy, “Quantification of Vessel Density in Retinal Optical Coherence Tomography Angiography Images Using Local Fractal Dimension,” Invest. Ophthalmol. Vis. Sci. 57(1), 246–252 (2016).
[Crossref] [PubMed]

Bianconi, F.

J. N. Kather, C.-A. Weis, F. Bianconi, S. M. Melchers, L. R. Schad, T. Gaiser, A. Marx, and F. G. Zöllner, “Multi-class texture analysis in colorectal cancer histology,” Sci. Rep. 6(1), 27988 (2016).
[Crossref] [PubMed]

Bonanomi, M. T.

M. T. Bonanomi and M. M. Lavezzo, “Sickle cell retinopathy: diagnosis and treatment,” Arq. Bras. Oftalmol. 76(5), 320–327 (2013).
[Crossref] [PubMed]

Broe, R.

R. Broe, M. L. Rasmussen, U. Frydkjaer-Olsen, B. S. Olsen, H. B. Mortensen, T. Peto, and J. Grauslund, “Retinal vascular fractals predict long-term microvascular complications in type 1 diabetes mellitus: the Danish Cohort of Pediatric Diabetes 1987 (DCPD1987),” Diabetologia 57(10), 2215–2221 (2014).
[Crossref] [PubMed]

Busse, B.

G. K. Asdourian, K. C. Nagpal, B. Busse, M. Goldbaum, D. Patriankos, M. F. Rabb, and M. F. Goldberg, “Macular and perimacular vascular remodelling sickling haemoglobinopathies,” Br. J. Ophthalmol. 60(6), 431–453 (1976).
[Crossref] [PubMed]

Caillaux, V.

W. Minvielle, V. Caillaux, S. Y. Cohen, F. Chasset, O. Zambrowski, A. Miere, and E. H. Souied, “Macular Microangiopathy in Sickle Cell Disease Using Optical Coherence Tomography Angiography,” Am. J. Ophthalmol. 164, 137–144 (2016).
[Crossref] [PubMed]

Cano, J. R.

S. García, J. Derrac, J. R. Cano, and F. Herrera, “Prototype selection for nearest neighbor classification: Taxonomy and empirical study,” IEEE Trans. Pattern Anal. Mach. Intell. 34(3), 417–435 (2012).
[Crossref] [PubMed]

Cao, D.

Chasset, F.

W. Minvielle, V. Caillaux, S. Y. Cohen, F. Chasset, O. Zambrowski, A. Miere, and E. H. Souied, “Macular Microangiopathy in Sickle Cell Disease Using Optical Coherence Tomography Angiography,” Am. J. Ophthalmol. 164, 137–144 (2016).
[Crossref] [PubMed]

Chau, F. Y.

Q. V. Hoang, F. Y. Chau, M. Shahidi, and J. I. Lim, “Central macular splaying and outer retinal thinning in asymptomatic sickle cell patients by spectral-domain optical coherence tomography,” Am. J. Ophthalmol. 151, 990–994 (2011).

Chen, C. L.

Z. Chu, J. Lin, C. Gao, C. Xin, Q. Zhang, C. L. Chen, L. Roisman, G. Gregori, P. J. Rosenfeld, and R. K. Wang, “Quantitative assessment of the retinal microvasculature using optical coherence tomography angiography,” J. Biomed. Opt. 21(6), 066008 (2016).
[Crossref] [PubMed]

Chidambara, L.

S. G. K. Gadde, N. Anegondi, D. Bhanushali, L. Chidambara, N. K. Yadav, A. Khurana, and A. Sinha Roy, “Quantification of Vessel Density in Retinal Optical Coherence Tomography Angiography Images Using Local Fractal Dimension,” Invest. Ophthalmol. Vis. Sci. 57(1), 246–252 (2016).
[Crossref] [PubMed]

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Gurgel, R. Q.

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Jain, R.

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B. Aliahmad, D. K. Kumar, M. G. Sarossy, and R. Jain, “Relationship between diabetes and grayscale fractal dimensions of retinal vasculature in the Indian population,” BMC Ophthalmol. 14(1), 152 (2014).
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T. S. Hwang, Y. Jia, S. S. Gao, S. T. Bailey, A. K. Lauer, C. J. Flaxel, D. J. Wilson, and D. Huang, “Optical coherence tomography angiography features of diabetic retinopathy,” Retina 35(11), 2371–2376 (2015).
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Lin, J.

Z. Chu, J. Lin, C. Gao, C. Xin, Q. Zhang, C. L. Chen, L. Roisman, G. Gregori, P. J. Rosenfeld, and R. K. Wang, “Quantitative assessment of the retinal microvasculature using optical coherence tomography angiography,” J. Biomed. Opt. 21(6), 066008 (2016).
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Miere, A.

W. Minvielle, V. Caillaux, S. Y. Cohen, F. Chasset, O. Zambrowski, A. Miere, and E. H. Souied, “Macular Microangiopathy in Sickle Cell Disease Using Optical Coherence Tomography Angiography,” Am. J. Ophthalmol. 164, 137–144 (2016).
[Crossref] [PubMed]

Minvielle, W.

W. Minvielle, V. Caillaux, S. Y. Cohen, F. Chasset, O. Zambrowski, A. Miere, and E. H. Souied, “Macular Microangiopathy in Sickle Cell Disease Using Optical Coherence Tomography Angiography,” Am. J. Ophthalmol. 164, 137–144 (2016).
[Crossref] [PubMed]

Mortensen, H. B.

R. Broe, M. L. Rasmussen, U. Frydkjaer-Olsen, B. S. Olsen, H. B. Mortensen, T. Peto, and J. Grauslund, “Retinal vascular fractals predict long-term microvascular complications in type 1 diabetes mellitus: the Danish Cohort of Pediatric Diabetes 1987 (DCPD1987),” Diabetologia 57(10), 2215–2221 (2014).
[Crossref] [PubMed]

Moult, E.

E. Moult, W. Choi, N. K. Waheed, M. Adhi, B. Lee, C. D. Lu, V. Jayaraman, B. Potsaid, P. J. Rosenfeld, J. S. Duker, and J. G. Fujimoto, “Ultrahigh-speed swept-source OCT angiography in exudative AMD,” Ophthalmic Surg. Lasers Imaging Retina 45(6), 496–505 (2014).
[Crossref] [PubMed]

Nagpal, K. C.

G. K. Asdourian, K. C. Nagpal, B. Busse, M. Goldbaum, D. Patriankos, M. F. Rabb, and M. F. Goldberg, “Macular and perimacular vascular remodelling sickling haemoglobinopathies,” Br. J. Ophthalmol. 60(6), 431–453 (1976).
[Crossref] [PubMed]

Nelson, M. R.

W. E. Hart, M. Goldbaum, B. Côté, P. Kube, and M. R. Nelson, “Measurement and classification of retinal vascular tortuosity,” Int. J. Med. Inform. 53(2-3), 239–252 (1999).
[Crossref] [PubMed]

Olsen, B. S.

R. Broe, M. L. Rasmussen, U. Frydkjaer-Olsen, B. S. Olsen, H. B. Mortensen, T. Peto, and J. Grauslund, “Retinal vascular fractals predict long-term microvascular complications in type 1 diabetes mellitus: the Danish Cohort of Pediatric Diabetes 1987 (DCPD1987),” Diabetologia 57(10), 2215–2221 (2014).
[Crossref] [PubMed]

Parrot, J.-F.

H. Taud and J.-F. Parrot, “Measurement of DEM roughness using the local fractal dimension,” G’eomorphologie 11(4), 327–338 (2005).
[Crossref]

Patriankos, D.

G. K. Asdourian, K. C. Nagpal, B. Busse, M. Goldbaum, D. Patriankos, M. F. Rabb, and M. F. Goldberg, “Macular and perimacular vascular remodelling sickling haemoglobinopathies,” Br. J. Ophthalmol. 60(6), 431–453 (1976).
[Crossref] [PubMed]

Pennesi, M. E.

Y. Jia, S. T. Bailey, T. S. Hwang, S. M. McClintic, S. S. Gao, M. E. Pennesi, C. J. Flaxel, A. K. Lauer, D. J. Wilson, J. Hornegger, J. G. Fujimoto, and D. Huang, “Quantitative optical coherence tomography angiography of vascular abnormalities in the living human eye,” Proc. Natl. Acad. Sci. U.S.A. 112(18), E2395–E2402 (2015).
[Crossref] [PubMed]

Peto, T.

R. Broe, M. L. Rasmussen, U. Frydkjaer-Olsen, B. S. Olsen, H. B. Mortensen, T. Peto, and J. Grauslund, “Retinal vascular fractals predict long-term microvascular complications in type 1 diabetes mellitus: the Danish Cohort of Pediatric Diabetes 1987 (DCPD1987),” Diabetologia 57(10), 2215–2221 (2014).
[Crossref] [PubMed]

Potsaid, B.

E. Moult, W. Choi, N. K. Waheed, M. Adhi, B. Lee, C. D. Lu, V. Jayaraman, B. Potsaid, P. J. Rosenfeld, J. S. Duker, and J. G. Fujimoto, “Ultrahigh-speed swept-source OCT angiography in exudative AMD,” Ophthalmic Surg. Lasers Imaging Retina 45(6), 496–505 (2014).
[Crossref] [PubMed]

Pujol, O.

S. Escalera, O. Pujol, and P. Radeva, “On the decoding process in ternary error-correcting output codes,” IEEE Trans. Pattern Anal. Mach. Intell. 32(1), 120–134 (2010).
[Crossref] [PubMed]

Rabb, M. F.

G. K. Asdourian, K. C. Nagpal, B. Busse, M. Goldbaum, D. Patriankos, M. F. Rabb, and M. F. Goldberg, “Macular and perimacular vascular remodelling sickling haemoglobinopathies,” Br. J. Ophthalmol. 60(6), 431–453 (1976).
[Crossref] [PubMed]

Radeva, P.

S. Escalera, O. Pujol, and P. Radeva, “On the decoding process in ternary error-correcting output codes,” IEEE Trans. Pattern Anal. Mach. Intell. 32(1), 120–134 (2010).
[Crossref] [PubMed]

Rasmussen, M. L.

R. Broe, M. L. Rasmussen, U. Frydkjaer-Olsen, B. S. Olsen, H. B. Mortensen, T. Peto, and J. Grauslund, “Retinal vascular fractals predict long-term microvascular complications in type 1 diabetes mellitus: the Danish Cohort of Pediatric Diabetes 1987 (DCPD1987),” Diabetologia 57(10), 2215–2221 (2014).
[Crossref] [PubMed]

Roisman, L.

Z. Chu, J. Lin, C. Gao, C. Xin, Q. Zhang, C. L. Chen, L. Roisman, G. Gregori, P. J. Rosenfeld, and R. K. Wang, “Quantitative assessment of the retinal microvasculature using optical coherence tomography angiography,” J. Biomed. Opt. 21(6), 066008 (2016).
[Crossref] [PubMed]

Rosenfeld, P. J.

Z. Chu, J. Lin, C. Gao, C. Xin, Q. Zhang, C. L. Chen, L. Roisman, G. Gregori, P. J. Rosenfeld, and R. K. Wang, “Quantitative assessment of the retinal microvasculature using optical coherence tomography angiography,” J. Biomed. Opt. 21(6), 066008 (2016).
[Crossref] [PubMed]

E. Moult, W. Choi, N. K. Waheed, M. Adhi, B. Lee, C. D. Lu, V. Jayaraman, B. Potsaid, P. J. Rosenfeld, J. S. Duker, and J. G. Fujimoto, “Ultrahigh-speed swept-source OCT angiography in exudative AMD,” Ophthalmic Surg. Lasers Imaging Retina 45(6), 496–505 (2014).
[Crossref] [PubMed]

Salifoglou, A.

I. Kavakiotis, O. Tsave, A. Salifoglou, N. Maglaveras, I. Vlahavas, and I. Chouvarda, “Machine learning and data mining methods in diabetes research,” Comput. Struct. Biotechnol. J. 15, 104–116 (2017).
[Crossref] [PubMed]

Sarossy, M. G.

B. Aliahmad, D. K. Kumar, M. G. Sarossy, and R. Jain, “Relationship between diabetes and grayscale fractal dimensions of retinal vasculature in the Indian population,” BMC Ophthalmol. 14(1), 152 (2014).
[Crossref] [PubMed]

Schad, L. R.

J. N. Kather, C.-A. Weis, F. Bianconi, S. M. Melchers, L. R. Schad, T. Gaiser, A. Marx, and F. G. Zöllner, “Multi-class texture analysis in colorectal cancer histology,” Sci. Rep. 6(1), 27988 (2016).
[Crossref] [PubMed]

Schapire, R. E.

E. L. Allwein, R. E. Schapire, and Y. Singer, “Reducing multiclass to binary: A unifying approach for margin classifiers,” J. Mach. Learn. Res. 1, 113–141 (2000).

Sebastiani, P.

N. Solovieff, S. W. Hartley, C. T. Baldwin, E. S. Klings, M. T. Gladwin, J. G. Taylor, G. J. Kato, L. A. Farrer, M. H. Steinberg, and P. Sebastiani, “Ancestry of African Americans with Sickle Cell Disease,” Blood Cells Mol. Dis. 47(1), 41–45 (2011).
[Crossref] [PubMed]

Serjeant, G. R.

P. I. Condon and G. R. Serjeant, “Ocular Findings in Homozygous Sickle Cell Anemia in Jamaica,” Am. J. Ophthalmol. 73(4), 533–543 (1972).
[Crossref] [PubMed]

Shahidi, M.

Q. V. Hoang, F. Y. Chau, M. Shahidi, and J. I. Lim, “Central macular splaying and outer retinal thinning in asymptomatic sickle cell patients by spectral-domain optical coherence tomography,” Am. J. Ophthalmol. 151, 990–994 (2011).

Shaw, J.

J. W. Yau, R. Kawasaki, F. M. Islam, J. Shaw, P. Zimmet, J. J. Wang, and T. Y. Wong, “Retinal fractal dimension is increased in persons with diabetes but not impaired glucose metabolism: the Australian Diabetes, Obesity and Lifestyle (AusDiab) study,” Diabetologia 53(9), 2042–2045 (2010).
[Crossref] [PubMed]

Singer, Y.

E. L. Allwein, R. E. Schapire, and Y. Singer, “Reducing multiclass to binary: A unifying approach for margin classifiers,” J. Mach. Learn. Res. 1, 113–141 (2000).

Sinha Roy, A.

S. G. K. Gadde, N. Anegondi, D. Bhanushali, L. Chidambara, N. K. Yadav, A. Khurana, and A. Sinha Roy, “Quantification of Vessel Density in Retinal Optical Coherence Tomography Angiography Images Using Local Fractal Dimension,” Invest. Ophthalmol. Vis. Sci. 57(1), 246–252 (2016).
[Crossref] [PubMed]

Smith, E. W.

E. W. Smith and C. L. Conley, “Clinical features of the genetic variants of sickle cell disease,” Bull. Johns Hopkins Hosp. 94(6), 289–318 (1954).
[PubMed]

Solovieff, N.

N. Solovieff, S. W. Hartley, C. T. Baldwin, E. S. Klings, M. T. Gladwin, J. G. Taylor, G. J. Kato, L. A. Farrer, M. H. Steinberg, and P. Sebastiani, “Ancestry of African Americans with Sickle Cell Disease,” Blood Cells Mol. Dis. 47(1), 41–45 (2011).
[Crossref] [PubMed]

Souied, E. H.

W. Minvielle, V. Caillaux, S. Y. Cohen, F. Chasset, O. Zambrowski, A. Miere, and E. H. Souied, “Macular Microangiopathy in Sickle Cell Disease Using Optical Coherence Tomography Angiography,” Am. J. Ophthalmol. 164, 137–144 (2016).
[Crossref] [PubMed]

Spaide, R. F.

R. F. Spaide and C. A. Curcio, “Evaluation of Segmentation of the Superficial and Deep Vascular Layers of the Retina by Optical Coherence Tomography Angiography Instruments in Normal Eyes,” JAMA Ophthalmol. 135(3), 259–262 (2017).
[Crossref] [PubMed]

Steinberg, M. H.

N. Solovieff, S. W. Hartley, C. T. Baldwin, E. S. Klings, M. T. Gladwin, J. G. Taylor, G. J. Kato, L. A. Farrer, M. H. Steinberg, and P. Sebastiani, “Ancestry of African Americans with Sickle Cell Disease,” Blood Cells Mol. Dis. 47(1), 41–45 (2011).
[Crossref] [PubMed]

Taud, H.

H. Taud and J.-F. Parrot, “Measurement of DEM roughness using the local fractal dimension,” G’eomorphologie 11(4), 327–338 (2005).
[Crossref]

Taylor, J. G.

N. Solovieff, S. W. Hartley, C. T. Baldwin, E. S. Klings, M. T. Gladwin, J. G. Taylor, G. J. Kato, L. A. Farrer, M. H. Steinberg, and P. Sebastiani, “Ancestry of African Americans with Sickle Cell Disease,” Blood Cells Mol. Dis. 47(1), 41–45 (2011).
[Crossref] [PubMed]

Thapa, D.

Tsave, O.

I. Kavakiotis, O. Tsave, A. Salifoglou, N. Maglaveras, I. Vlahavas, and I. Chouvarda, “Machine learning and data mining methods in diabetes research,” Comput. Struct. Biotechnol. J. 15, 104–116 (2017).
[Crossref] [PubMed]

Vihinen, M.

M. Vihinen, “How to evaluate performance of prediction methods? Measures and their interpretation in variation effect analysis,” BMC Genomics 13(4Suppl 4), S2 (2012).
[Crossref] [PubMed]

Vlahavas, I.

I. Kavakiotis, O. Tsave, A. Salifoglou, N. Maglaveras, I. Vlahavas, and I. Chouvarda, “Machine learning and data mining methods in diabetes research,” Comput. Struct. Biotechnol. J. 15, 104–116 (2017).
[Crossref] [PubMed]

Von Sallmann, L.

G. Goodman, L. Von Sallmann, and M. G. Holland, “Ocular manifestations of sickle-cell disease,” AMA Arch. Opthalmol. 58(5), 655–682 (1957).
[Crossref] [PubMed]

Waheed, N. K.

E. Moult, W. Choi, N. K. Waheed, M. Adhi, B. Lee, C. D. Lu, V. Jayaraman, B. Potsaid, P. J. Rosenfeld, J. S. Duker, and J. G. Fujimoto, “Ultrahigh-speed swept-source OCT angiography in exudative AMD,” Ophthalmic Surg. Lasers Imaging Retina 45(6), 496–505 (2014).
[Crossref] [PubMed]

Wang, J. J.

J. W. Yau, R. Kawasaki, F. M. Islam, J. Shaw, P. Zimmet, J. J. Wang, and T. Y. Wong, “Retinal fractal dimension is increased in persons with diabetes but not impaired glucose metabolism: the Australian Diabetes, Obesity and Lifestyle (AusDiab) study,” Diabetologia 53(9), 2042–2045 (2010).
[Crossref] [PubMed]

Wang, R. K.

Z. Chu, J. Lin, C. Gao, C. Xin, Q. Zhang, C. L. Chen, L. Roisman, G. Gregori, P. J. Rosenfeld, and R. K. Wang, “Quantitative assessment of the retinal microvasculature using optical coherence tomography angiography,” J. Biomed. Opt. 21(6), 066008 (2016).
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R. K. Wang, S. L. Jacques, Z. Ma, S. Hurst, S. R. Hanson, and A. Gruber, “Three dimensional optical angiography,” Opt. Express 15(7), 4083–4097 (2007).
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Weis, C.-A.

J. N. Kather, C.-A. Weis, F. Bianconi, S. M. Melchers, L. R. Schad, T. Gaiser, A. Marx, and F. G. Zöllner, “Multi-class texture analysis in colorectal cancer histology,” Sci. Rep. 6(1), 27988 (2016).
[Crossref] [PubMed]

Wilson, D. J.

Y. Jia, S. T. Bailey, T. S. Hwang, S. M. McClintic, S. S. Gao, M. E. Pennesi, C. J. Flaxel, A. K. Lauer, D. J. Wilson, J. Hornegger, J. G. Fujimoto, and D. Huang, “Quantitative optical coherence tomography angiography of vascular abnormalities in the living human eye,” Proc. Natl. Acad. Sci. U.S.A. 112(18), E2395–E2402 (2015).
[Crossref] [PubMed]

T. S. Hwang, Y. Jia, S. S. Gao, S. T. Bailey, A. K. Lauer, C. J. Flaxel, D. J. Wilson, and D. Huang, “Optical coherence tomography angiography features of diabetic retinopathy,” Retina 35(11), 2371–2376 (2015).
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Wong, T. Y.

J. W. Yau, R. Kawasaki, F. M. Islam, J. Shaw, P. Zimmet, J. J. Wang, and T. Y. Wong, “Retinal fractal dimension is increased in persons with diabetes but not impaired glucose metabolism: the Australian Diabetes, Obesity and Lifestyle (AusDiab) study,” Diabetologia 53(9), 2042–2045 (2010).
[Crossref] [PubMed]

Xin, C.

Z. Chu, J. Lin, C. Gao, C. Xin, Q. Zhang, C. L. Chen, L. Roisman, G. Gregori, P. J. Rosenfeld, and R. K. Wang, “Quantitative assessment of the retinal microvasculature using optical coherence tomography angiography,” J. Biomed. Opt. 21(6), 066008 (2016).
[Crossref] [PubMed]

Yadav, N. K.

S. G. K. Gadde, N. Anegondi, D. Bhanushali, L. Chidambara, N. K. Yadav, A. Khurana, and A. Sinha Roy, “Quantification of Vessel Density in Retinal Optical Coherence Tomography Angiography Images Using Local Fractal Dimension,” Invest. Ophthalmol. Vis. Sci. 57(1), 246–252 (2016).
[Crossref] [PubMed]

Yao, X.

Yau, J. W.

J. W. Yau, R. Kawasaki, F. M. Islam, J. Shaw, P. Zimmet, J. J. Wang, and T. Y. Wong, “Retinal fractal dimension is increased in persons with diabetes but not impaired glucose metabolism: the Australian Diabetes, Obesity and Lifestyle (AusDiab) study,” Diabetologia 53(9), 2042–2045 (2010).
[Crossref] [PubMed]

Zambrowski, O.

W. Minvielle, V. Caillaux, S. Y. Cohen, F. Chasset, O. Zambrowski, A. Miere, and E. H. Souied, “Macular Microangiopathy in Sickle Cell Disease Using Optical Coherence Tomography Angiography,” Am. J. Ophthalmol. 164, 137–144 (2016).
[Crossref] [PubMed]

Zhang, Q.

Z. Chu, J. Lin, C. Gao, C. Xin, Q. Zhang, C. L. Chen, L. Roisman, G. Gregori, P. J. Rosenfeld, and R. K. Wang, “Quantitative assessment of the retinal microvasculature using optical coherence tomography angiography,” J. Biomed. Opt. 21(6), 066008 (2016).
[Crossref] [PubMed]

Zimmet, P.

J. W. Yau, R. Kawasaki, F. M. Islam, J. Shaw, P. Zimmet, J. J. Wang, and T. Y. Wong, “Retinal fractal dimension is increased in persons with diabetes but not impaired glucose metabolism: the Australian Diabetes, Obesity and Lifestyle (AusDiab) study,” Diabetologia 53(9), 2042–2045 (2010).
[Crossref] [PubMed]

Zöllner, F. G.

J. N. Kather, C.-A. Weis, F. Bianconi, S. M. Melchers, L. R. Schad, T. Gaiser, A. Marx, and F. G. Zöllner, “Multi-class texture analysis in colorectal cancer histology,” Sci. Rep. 6(1), 27988 (2016).
[Crossref] [PubMed]

Am. J. Ophthalmol. (4)

P. I. Condon and G. R. Serjeant, “Ocular Findings in Homozygous Sickle Cell Anemia in Jamaica,” Am. J. Ophthalmol. 73(4), 533–543 (1972).
[Crossref] [PubMed]

M. H. Goldbaum, “Retinal Depression Sign Indicating a Small Retinal Infarct,” Am. J. Ophthalmol. 86(1), 45–55 (1978).
[Crossref] [PubMed]

Q. V. Hoang, F. Y. Chau, M. Shahidi, and J. I. Lim, “Central macular splaying and outer retinal thinning in asymptomatic sickle cell patients by spectral-domain optical coherence tomography,” Am. J. Ophthalmol. 151, 990–994 (2011).

W. Minvielle, V. Caillaux, S. Y. Cohen, F. Chasset, O. Zambrowski, A. Miere, and E. H. Souied, “Macular Microangiopathy in Sickle Cell Disease Using Optical Coherence Tomography Angiography,” Am. J. Ophthalmol. 164, 137–144 (2016).
[Crossref] [PubMed]

AMA Arch. Opthalmol. (1)

G. Goodman, L. Von Sallmann, and M. G. Holland, “Ocular manifestations of sickle-cell disease,” AMA Arch. Opthalmol. 58(5), 655–682 (1957).
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Ann. Trop. Paediatr. (1)

A. O. Fadugbagbe, R. Q. Gurgel, C. Q. Mendonça, R. Cipolotti, A. M. dos Santos, and L. E. Cuevas, “Ocular manifestations of sickle cell disease,” Ann. Trop. Paediatr. 30(1), 19–26 (2010).
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Arch. Ophthalmol. (1)

M. H. Goldbaum, L. M. Jampol, and M. F. Goldberg, “The disc sign in sickling hemoglobinopathies,” Arch. Ophthalmol. 96(9), 1597–1600 (1978).
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Arq. Bras. Oftalmol. (1)

M. T. Bonanomi and M. M. Lavezzo, “Sickle cell retinopathy: diagnosis and treatment,” Arq. Bras. Oftalmol. 76(5), 320–327 (2013).
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Biomed. Opt. Express (1)

Blood Cells Mol. Dis. (1)

N. Solovieff, S. W. Hartley, C. T. Baldwin, E. S. Klings, M. T. Gladwin, J. G. Taylor, G. J. Kato, L. A. Farrer, M. H. Steinberg, and P. Sebastiani, “Ancestry of African Americans with Sickle Cell Disease,” Blood Cells Mol. Dis. 47(1), 41–45 (2011).
[Crossref] [PubMed]

BMC Genomics (1)

M. Vihinen, “How to evaluate performance of prediction methods? Measures and their interpretation in variation effect analysis,” BMC Genomics 13(4Suppl 4), S2 (2012).
[Crossref] [PubMed]

BMC Ophthalmol. (1)

B. Aliahmad, D. K. Kumar, M. G. Sarossy, and R. Jain, “Relationship between diabetes and grayscale fractal dimensions of retinal vasculature in the Indian population,” BMC Ophthalmol. 14(1), 152 (2014).
[Crossref] [PubMed]

Br. J. Ophthalmol. (1)

G. K. Asdourian, K. C. Nagpal, B. Busse, M. Goldbaum, D. Patriankos, M. F. Rabb, and M. F. Goldberg, “Macular and perimacular vascular remodelling sickling haemoglobinopathies,” Br. J. Ophthalmol. 60(6), 431–453 (1976).
[Crossref] [PubMed]

Bull. Johns Hopkins Hosp. (1)

E. W. Smith and C. L. Conley, “Clinical features of the genetic variants of sickle cell disease,” Bull. Johns Hopkins Hosp. 94(6), 289–318 (1954).
[PubMed]

Comput. Struct. Biotechnol. J. (1)

I. Kavakiotis, O. Tsave, A. Salifoglou, N. Maglaveras, I. Vlahavas, and I. Chouvarda, “Machine learning and data mining methods in diabetes research,” Comput. Struct. Biotechnol. J. 15, 104–116 (2017).
[Crossref] [PubMed]

Curr. Opin. Ophthalmol. (1)

J. I. Lim, “Ophthalmic manifestations of sickle cell disease: update of the latest findings,” Curr. Opin. Ophthalmol. 23(6), 533–536 (2012).
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Diabetologia (2)

R. Broe, M. L. Rasmussen, U. Frydkjaer-Olsen, B. S. Olsen, H. B. Mortensen, T. Peto, and J. Grauslund, “Retinal vascular fractals predict long-term microvascular complications in type 1 diabetes mellitus: the Danish Cohort of Pediatric Diabetes 1987 (DCPD1987),” Diabetologia 57(10), 2215–2221 (2014).
[Crossref] [PubMed]

J. W. Yau, R. Kawasaki, F. M. Islam, J. Shaw, P. Zimmet, J. J. Wang, and T. Y. Wong, “Retinal fractal dimension is increased in persons with diabetes but not impaired glucose metabolism: the Australian Diabetes, Obesity and Lifestyle (AusDiab) study,” Diabetologia 53(9), 2042–2045 (2010).
[Crossref] [PubMed]

G’eomorphologie (1)

H. Taud and J.-F. Parrot, “Measurement of DEM roughness using the local fractal dimension,” G’eomorphologie 11(4), 327–338 (2005).
[Crossref]

Hematol. Rep. (1)

O. O. Ilesanmi, “Pathological basis of symptoms and crises in sickle cell disorder: implications for counseling and psychotherapy,” Hematol. Rep. 2(1), e2 (2010).
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IEEE Trans. Pattern Anal. Mach. Intell. (2)

S. García, J. Derrac, J. R. Cano, and F. Herrera, “Prototype selection for nearest neighbor classification: Taxonomy and empirical study,” IEEE Trans. Pattern Anal. Mach. Intell. 34(3), 417–435 (2012).
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S. Escalera, O. Pujol, and P. Radeva, “On the decoding process in ternary error-correcting output codes,” IEEE Trans. Pattern Anal. Mach. Intell. 32(1), 120–134 (2010).
[Crossref] [PubMed]

Int. J. Med. Inform. (1)

W. E. Hart, M. Goldbaum, B. Côté, P. Kube, and M. R. Nelson, “Measurement and classification of retinal vascular tortuosity,” Int. J. Med. Inform. 53(2-3), 239–252 (1999).
[Crossref] [PubMed]

Invest. Ophthalmol. Vis. Sci. (2)

R. Hu and C. Ding, “Quantification of Vessel Density in Retinal Optical Coherence Tomography Angiography Images Using Local Fractal Dimension,” Invest. Ophthalmol. Vis. Sci. 57(4), 2262 (2016).
[Crossref] [PubMed]

S. G. K. Gadde, N. Anegondi, D. Bhanushali, L. Chidambara, N. K. Yadav, A. Khurana, and A. Sinha Roy, “Quantification of Vessel Density in Retinal Optical Coherence Tomography Angiography Images Using Local Fractal Dimension,” Invest. Ophthalmol. Vis. Sci. 57(1), 246–252 (2016).
[Crossref] [PubMed]

J. Biomed. Opt. (1)

Z. Chu, J. Lin, C. Gao, C. Xin, Q. Zhang, C. L. Chen, L. Roisman, G. Gregori, P. J. Rosenfeld, and R. K. Wang, “Quantitative assessment of the retinal microvasculature using optical coherence tomography angiography,” J. Biomed. Opt. 21(6), 066008 (2016).
[Crossref] [PubMed]

J. Mach. Learn. Res. (1)

E. L. Allwein, R. E. Schapire, and Y. Singer, “Reducing multiclass to binary: A unifying approach for margin classifiers,” J. Mach. Learn. Res. 1, 113–141 (2000).

JAMA Ophthalmol. (1)

R. F. Spaide and C. A. Curcio, “Evaluation of Segmentation of the Superficial and Deep Vascular Layers of the Retina by Optical Coherence Tomography Angiography Instruments in Normal Eyes,” JAMA Ophthalmol. 135(3), 259–262 (2017).
[Crossref] [PubMed]

Mach. Learn. (1)

T. Joachims, “Text categorization with support vector machines: Learning with many relevant features,” Mach. Learn. ECML-98, 137–142 (1998).

Ophthalmic Surg. Lasers Imaging Retina (1)

E. Moult, W. Choi, N. K. Waheed, M. Adhi, B. Lee, C. D. Lu, V. Jayaraman, B. Potsaid, P. J. Rosenfeld, J. S. Duker, and J. G. Fujimoto, “Ultrahigh-speed swept-source OCT angiography in exudative AMD,” Ophthalmic Surg. Lasers Imaging Retina 45(6), 496–505 (2014).
[Crossref] [PubMed]

Opt. Express (1)

Proc. Natl. Acad. Sci. U.S.A. (1)

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Figures (4)

Fig. 1
Fig. 1 Flow chart of the procedures for automated classification.
Fig. 2
Fig. 2 Representative OCTA images of superficial (a-c) and deep (e-g) layers. (a,e) Control eyes, (b,f) Mild stage SCR, (c,g) Severe stage SCR. (d) and (h) show corresponding sample B-scan OCT images with segmented superficial and deep layers respectively. (a-c) and (e-g) have same scale bar. (d) and (h) have same scale bar.
Fig. 3
Fig. 3 A flow chart showing various features extracted from OCTA image.
Fig. 4
Fig. 4 Representative images for illustrating the feature extraction (a) OCTA raw image, (b) Segmented large blood vessel map, (c) Skeletonized blood vessels branches with identified endpoints (for a random vessel branch, A and B endpoints are shown with red dots), (d) Vessel perimeter map, (e) Segmented avascular region, (f) FAZ contour, (g,h) Contour maps created with normalized values of local fractal dimension in superficial and deep layers respectively. (g) Circular zones of diameter 2, 4 and 6mm, (h) Nasal, Superior, Temporal and Inferior regions.

Tables (3)

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Table 1 Methodology for extracting features.

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Table 2 Performance comparison between single and combined features

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Table 3 Performance analysis of three classifiers (using all 6 parameters)

Equations (3)

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Sensitivity=   A A+C
Specificity=   D B+D
Accuracy=   A+D A+B+C+D

Metrics