Abstract

Early detection is an essential step for effective intervention of sickle cell retinopathy (SCR). Emerging optical coherence tomography angiography (OCTA) provides excellent three-dimensional (3D) resolution to enable label-free, noninvasive visualization of retinal vascular structures, promising improved sensitivity in detecting SCR. However, quantitative analysis of SCR characteristics in OCTA images is yet to be established. In this study, we conducted comprehensive analysis of six OCTA parameters, including blood vessel tortuosity, vessel diameter, vessel perimeter index (VPI), area of foveal avascular zone (FAZ), contour irregularity of FAZ and parafoveal avascular density. Compared to traditional retinal thickness analysis, five of these six OCTA parameters show improved sensitivity for SCR detection than retinal thickness. It is observed that the most sensitive parameters were the contour irregularity of FAZ in the superficial layer and avascular density in temporal regions, while the area of FAZ, tortuosity and mean diameter of the vessel were moderately sensitive.

© 2017 Optical Society of America

Full Article  |  PDF Article
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References

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2016 (3)

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]

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]

S. G. 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]

2015 (3)

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]

A. Zhang, Q. Zhang, and R. K. Wang, “Minimizing projection artifacts for accurate presentation of choroidal neovascularization in OCT micro-angiography,” Biomed. Opt. Express 6(10), 4130–4143 (2015).
[Crossref] [PubMed]

2014 (3)

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]

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]

2012 (2)

2011 (2)

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(6), 990–994 (2011).
[Crossref] [PubMed]

S. K. Alam, E. J. Feleppa, M. Rondeau, A. Kalisz, and B. S. Garra, “Ultrasonic multi-feature analysis procedure for computer-aided diagnosis of solid breast lesions,” Ultrason. Imaging 33(1), 17–38 (2011).
[Crossref] [PubMed]

2010 (2)

J. W. Yau and R. Kawasaki, “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).

K. L. Hassell, “Population estimates of sickle cell disease in the U.S,” Am. J. Prev. Med. 38(4Suppl), S512–S521 (2010).
[Crossref] [PubMed]

2008 (1)

O. S. Al-Kadi and D. Watson, “Texture analysis of aggressive and nonaggressive lung tumor CE CT images,” IEEE Trans. Biomed. Eng. 55(7), 1822–1830 (2008).
[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]

2001 (1)

T. F. Chan and L. A. Vese, “Active contours without edges,” IEEE Trans. Image Process. 10(2), 266–277 (2001).
[Crossref] [PubMed]

2000 (1)

T. F. Chan, B. Y. Sandberg, and L. A. Vese, “Active contours without edges for vector-valued images,” J. Vis. Commun. Image Represent. 11(2), 130–141 (2000).
[Crossref]

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]

1994 (2)

L. Zhou, M. S. Rzeszotarski, L. J. Singerman, and J. M. Chokreff, “The detection and quantification of retinopathy using digital angiograms,” IEEE Trans. Med. Imaging 13(4), 619–626 (1994).
[Crossref] [PubMed]

M. H. Goldbaum, W. E. Hart, B. L. Cote, and P. V. Raphaelian, “Automated measures of retinal blood vessel tortuosity,” Invest. Ophthalmol. Vis. Sci. 35, 2089 (1994).

1993 (1)

O. Smedby, N. Högman, S. Nilsson, U. Erikson, A. G. Olsson, and G. Walldius, “Two-dimensional tortuosity of the superficial femoral artery in early atherosclerosis,” J. Vasc. Res. 30(4), 181–191 (1993).
[Crossref] [PubMed]

1992 (1)

L. Lam, S.-W. Lee, and C. Y. Suen, “Thinning methodologies-a comprehensive survey,” IEEE Trans. Pattern Anal. Mach. Intell. 14(9), 869 (1992).
[Crossref]

1982 (1)

D. Bracher, “Changes in peripapillary tortuosity of the central retinal arteries in newborns. A phenomenon whose underlying mechanisms need clarification,” Graefes Arch. Clin. Exp. Ophthalmol. 218(4), 211–217 (1982).
[Crossref] [PubMed]

1976 (2)

P. I. Condon and G. R. Serjeant, “Ocular findings of elderly cases of homozygous sickle-cell disease in Jamaica,” Br. J. Ophthalmol. 60(5), 361–364 (1976).
[Crossref] [PubMed]

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]

1971 (1)

M. F. Goldberg, “Classification and pathogenesis of proliferative sickle retinopathy,” Am. J. Ophthalmol. 71(3), 649–665 (1971).
[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]

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, S. K.

S. K. Alam, E. J. Feleppa, M. Rondeau, A. Kalisz, and B. S. Garra, “Ultrasonic multi-feature analysis procedure for computer-aided diagnosis of solid breast lesions,” Ultrason. Imaging 33(1), 17–38 (2011).
[Crossref] [PubMed]

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]

Al-Kadi, O. S.

O. S. Al-Kadi and D. Watson, “Texture analysis of aggressive and nonaggressive lung tumor CE CT images,” IEEE Trans. Biomed. Eng. 55(7), 1822–1830 (2008).
[Crossref] [PubMed]

Anegondi, N.

S. G. 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]

Bhanushali, D.

S. G. 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]

Bracher, D.

D. Bracher, “Changes in peripapillary tortuosity of the central retinal arteries in newborns. A phenomenon whose underlying mechanisms need clarification,” Graefes Arch. Clin. Exp. Ophthalmol. 218(4), 211–217 (1982).
[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]

Chan, T. F.

T. F. Chan and L. A. Vese, “Active contours without edges,” IEEE Trans. Image Process. 10(2), 266–277 (2001).
[Crossref] [PubMed]

T. F. Chan, B. Y. Sandberg, and L. A. Vese, “Active contours without edges for vector-valued images,” J. Vis. Commun. Image Represent. 11(2), 130–141 (2000).
[Crossref]

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(6), 990–994 (2011).
[Crossref] [PubMed]

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. 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]

Choi, W.

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]

Chokreff, J. M.

L. Zhou, M. S. Rzeszotarski, L. J. Singerman, and J. M. Chokreff, “The detection and quantification of retinopathy using digital angiograms,” IEEE Trans. Med. Imaging 13(4), 619–626 (1994).
[Crossref] [PubMed]

Chu, Z.

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]

Cohen, S. Y.

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]

Condon, P. I.

P. I. Condon and G. R. Serjeant, “Ocular findings of elderly cases of homozygous sickle-cell disease in Jamaica,” Br. J. Ophthalmol. 60(5), 361–364 (1976).
[Crossref] [PubMed]

Cote, B. L.

M. H. Goldbaum, W. E. Hart, B. L. Cote, and P. V. Raphaelian, “Automated measures of retinal blood vessel tortuosity,” Invest. Ophthalmol. Vis. Sci. 35, 2089 (1994).

Côté, B.

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]

Duker, J. S.

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]

Erikson, U.

O. Smedby, N. Högman, S. Nilsson, U. Erikson, A. G. Olsson, and G. Walldius, “Two-dimensional tortuosity of the superficial femoral artery in early atherosclerosis,” J. Vasc. Res. 30(4), 181–191 (1993).
[Crossref] [PubMed]

Feleppa, E. J.

S. K. Alam, E. J. Feleppa, M. Rondeau, A. Kalisz, and B. S. Garra, “Ultrasonic multi-feature analysis procedure for computer-aided diagnosis of solid breast lesions,” Ultrason. Imaging 33(1), 17–38 (2011).
[Crossref] [PubMed]

Flaxel, C. 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).
[Crossref] [PubMed]

Frydkjaer-Olsen, U.

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).
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Fujimoto, J. G.

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]

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]

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).
[Crossref] [PubMed]

Gadde, S. G.

S. G. 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]

Gao, 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]

Gao, S. S.

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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Garra, B. S.

S. K. Alam, E. J. Feleppa, M. Rondeau, A. Kalisz, and B. S. Garra, “Ultrasonic multi-feature analysis procedure for computer-aided diagnosis of solid breast lesions,” Ultrason. Imaging 33(1), 17–38 (2011).
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Goldbaum, M.

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).
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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).
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Goldbaum, M. H.

M. H. Goldbaum, W. E. Hart, B. L. Cote, and P. V. Raphaelian, “Automated measures of retinal blood vessel tortuosity,” Invest. Ophthalmol. Vis. Sci. 35, 2089 (1994).

Goldberg, 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).
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M. F. Goldberg, “Classification and pathogenesis of proliferative sickle retinopathy,” Am. J. Ophthalmol. 71(3), 649–665 (1971).
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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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Grauslund, J.

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]

Gregori, G.

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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Gruber, A.

Hanson, S. R.

Hart, W. E.

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).
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M. H. Goldbaum, W. E. Hart, B. L. Cote, and P. V. Raphaelian, “Automated measures of retinal blood vessel tortuosity,” Invest. Ophthalmol. Vis. Sci. 35, 2089 (1994).

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K. L. Hassell, “Population estimates of sickle cell disease in the U.S,” Am. J. Prev. Med. 38(4Suppl), S512–S521 (2010).
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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(6), 990–994 (2011).
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Högman, N.

O. Smedby, N. Högman, S. Nilsson, U. Erikson, A. G. Olsson, and G. Walldius, “Two-dimensional tortuosity of the superficial femoral artery in early atherosclerosis,” J. Vasc. Res. 30(4), 181–191 (1993).
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Holland, M. G.

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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Hornegger, 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]

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).
[Crossref] [PubMed]

Huang, D.

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]

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).
[Crossref] [PubMed]

Hurst, S.

Hwang, T. S.

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).
[Crossref] [PubMed]

Jacques, S. L.

Jain, R.

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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Jayaraman, V.

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).
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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).
[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]

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).
[Crossref] [PubMed]

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S. K. Alam, E. J. Feleppa, M. Rondeau, A. Kalisz, and B. S. Garra, “Ultrasonic multi-feature analysis procedure for computer-aided diagnosis of solid breast lesions,” Ultrason. Imaging 33(1), 17–38 (2011).
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Khurana, A.

S. G. 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).
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Kraus, M. F.

Kube, P.

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).
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Kumar, D. K.

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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L. Lam, S.-W. Lee, and C. Y. Suen, “Thinning methodologies-a comprehensive survey,” IEEE Trans. Pattern Anal. Mach. Intell. 14(9), 869 (1992).
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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).
[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).
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Lee, 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).
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Lee, S.-W.

L. Lam, S.-W. Lee, and C. Y. Suen, “Thinning methodologies-a comprehensive survey,” IEEE Trans. Pattern Anal. Mach. Intell. 14(9), 869 (1992).
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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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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(6), 990–994 (2011).
[Crossref] [PubMed]

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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Liu, J. J.

Lu, C. D.

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).
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Ma, Z.

McClintic, S. M.

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).
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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).
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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).
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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).
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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).
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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).
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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]

Nilsson, S.

O. Smedby, N. Högman, S. Nilsson, U. Erikson, A. G. Olsson, and G. Walldius, “Two-dimensional tortuosity of the superficial femoral artery in early atherosclerosis,” J. Vasc. Res. 30(4), 181–191 (1993).
[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).
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Olsson, A. G.

O. Smedby, N. Högman, S. Nilsson, U. Erikson, A. G. Olsson, and G. Walldius, “Two-dimensional tortuosity of the superficial femoral artery in early atherosclerosis,” J. Vasc. Res. 30(4), 181–191 (1993).
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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).
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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).
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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).
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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]

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).
[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]

Raphaelian, P. V.

M. H. Goldbaum, W. E. Hart, B. L. Cote, and P. V. Raphaelian, “Automated measures of retinal blood vessel tortuosity,” Invest. Ophthalmol. Vis. Sci. 35, 2089 (1994).

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).
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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]

Rondeau, M.

S. K. Alam, E. J. Feleppa, M. Rondeau, A. Kalisz, and B. S. Garra, “Ultrasonic multi-feature analysis procedure for computer-aided diagnosis of solid breast lesions,” Ultrason. Imaging 33(1), 17–38 (2011).
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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).
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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).
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Rzeszotarski, M. S.

L. Zhou, M. S. Rzeszotarski, L. J. Singerman, and J. M. Chokreff, “The detection and quantification of retinopathy using digital angiograms,” IEEE Trans. Med. Imaging 13(4), 619–626 (1994).
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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).
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P. I. Condon and G. R. Serjeant, “Ocular findings of elderly cases of homozygous sickle-cell disease in Jamaica,” Br. J. Ophthalmol. 60(5), 361–364 (1976).
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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(6), 990–994 (2011).
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Singerman, L. J.

L. Zhou, M. S. Rzeszotarski, L. J. Singerman, and J. M. Chokreff, “The detection and quantification of retinopathy using digital angiograms,” IEEE Trans. Med. Imaging 13(4), 619–626 (1994).
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Sinha Roy, A.

S. G. 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]

Smedby, O.

O. Smedby, N. Högman, S. Nilsson, U. Erikson, A. G. Olsson, and G. Walldius, “Two-dimensional tortuosity of the superficial femoral artery in early atherosclerosis,” J. Vasc. Res. 30(4), 181–191 (1993).
[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]

Subhash, H.

Suen, C. Y.

L. Lam, S.-W. Lee, and C. Y. Suen, “Thinning methodologies-a comprehensive survey,” IEEE Trans. Pattern Anal. Mach. Intell. 14(9), 869 (1992).
[Crossref]

Tan, O.

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]

Tokayer, J.

Vese, L. A.

T. F. Chan and L. A. Vese, “Active contours without edges,” IEEE Trans. Image Process. 10(2), 266–277 (2001).
[Crossref] [PubMed]

T. F. Chan, B. Y. Sandberg, and L. A. Vese, “Active contours without edges for vector-valued images,” J. Vis. Commun. Image Represent. 11(2), 130–141 (2000).
[Crossref]

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]

Walldius, G.

O. Smedby, N. Högman, S. Nilsson, U. Erikson, A. G. Olsson, and G. Walldius, “Two-dimensional tortuosity of the superficial femoral artery in early atherosclerosis,” J. Vasc. Res. 30(4), 181–191 (1993).
[Crossref] [PubMed]

Wang, R. K.

Wang, Y.

Watson, D.

O. S. Al-Kadi and D. Watson, “Texture analysis of aggressive and nonaggressive lung tumor CE CT images,” IEEE Trans. Biomed. Eng. 55(7), 1822–1830 (2008).
[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).
[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. 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]

Yau, J. W.

J. W. Yau and R. Kawasaki, “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).

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, A.

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]

A. Zhang, Q. Zhang, and R. K. Wang, “Minimizing projection artifacts for accurate presentation of choroidal neovascularization in OCT micro-angiography,” Biomed. Opt. Express 6(10), 4130–4143 (2015).
[Crossref] [PubMed]

Zhou, L.

L. Zhou, M. S. Rzeszotarski, L. J. Singerman, and J. M. Chokreff, “The detection and quantification of retinopathy using digital angiograms,” IEEE Trans. Med. Imaging 13(4), 619–626 (1994).
[Crossref] [PubMed]

Am. J. Ophthalmol. (3)

M. F. Goldberg, “Classification and pathogenesis of proliferative sickle retinopathy,” Am. J. Ophthalmol. 71(3), 649–665 (1971).
[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(6), 990–994 (2011).
[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]

Am. J. Prev. Med. (1)

K. L. Hassell, “Population estimates of sickle cell disease in the U.S,” Am. J. Prev. Med. 38(4Suppl), S512–S521 (2010).
[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).
[Crossref] [PubMed]

Biomed. Opt. Express (1)

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]

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P. I. Condon and G. R. Serjeant, “Ocular findings of elderly cases of homozygous sickle-cell disease in Jamaica,” Br. J. Ophthalmol. 60(5), 361–364 (1976).
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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]

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).
[Crossref] [PubMed]

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 and R. Kawasaki, “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).

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]

Graefes Arch. Clin. Exp. Ophthalmol. (1)

D. Bracher, “Changes in peripapillary tortuosity of the central retinal arteries in newborns. A phenomenon whose underlying mechanisms need clarification,” Graefes Arch. Clin. Exp. Ophthalmol. 218(4), 211–217 (1982).
[Crossref] [PubMed]

IEEE Trans. Biomed. Eng. (1)

O. S. Al-Kadi and D. Watson, “Texture analysis of aggressive and nonaggressive lung tumor CE CT images,” IEEE Trans. Biomed. Eng. 55(7), 1822–1830 (2008).
[Crossref] [PubMed]

IEEE Trans. Image Process. (1)

T. F. Chan and L. A. Vese, “Active contours without edges,” IEEE Trans. Image Process. 10(2), 266–277 (2001).
[Crossref] [PubMed]

IEEE Trans. Med. Imaging (1)

L. Zhou, M. S. Rzeszotarski, L. J. Singerman, and J. M. Chokreff, “The detection and quantification of retinopathy using digital angiograms,” IEEE Trans. Med. Imaging 13(4), 619–626 (1994).
[Crossref] [PubMed]

IEEE Trans. Pattern Anal. Mach. Intell. (1)

L. Lam, S.-W. Lee, and C. Y. Suen, “Thinning methodologies-a comprehensive survey,” IEEE Trans. Pattern Anal. Mach. Intell. 14(9), 869 (1992).
[Crossref]

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)

S. G. 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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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. Vasc. Res. (1)

O. Smedby, N. Högman, S. Nilsson, U. Erikson, A. G. Olsson, and G. Walldius, “Two-dimensional tortuosity of the superficial femoral artery in early atherosclerosis,” J. Vasc. Res. 30(4), 181–191 (1993).
[Crossref] [PubMed]

J. Vis. Commun. Image Represent. (1)

T. F. Chan, B. Y. Sandberg, and L. A. Vese, “Active contours without edges for vector-valued images,” J. Vis. Commun. Image Represent. 11(2), 130–141 (2000).
[Crossref]

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 (2)

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

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]

Retina (1)

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]

Ultrason. Imaging (1)

S. K. Alam, E. J. Feleppa, M. Rondeau, A. Kalisz, and B. S. Garra, “Ultrasonic multi-feature analysis procedure for computer-aided diagnosis of solid breast lesions,” Ultrason. Imaging 33(1), 17–38 (2011).
[Crossref] [PubMed]

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H. Azegrouz, “Thickness dependent tortuosity estimation for retinal blood vessels,” Engineering in Medicine and Biology Society, 2006. EMBS'06. 28th Annual International Conference of the IEEE (2006).
[Crossref]

Sickcel Cell Guideline Panel, “Sickle Cell Disease: Screening, Diagnosis, Management, and Counseling in Newborns and Infants,” AHCPR publication no. 93–0562 (Agency for Health Care Policy and Research, US Public Health Service, Rockville, MD: 1993).

Q. Zhang, “Projection Artifact Removal Improves Visualization and Quantitation of Macular Neovascularization Imaged by Optical Coherence Tomography Angiography ” Ophthalmology Retina (Posted 2 November 2016, In press).

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Figures (6)

Fig. 1
Fig. 1 Measuring tortuosity of OCTA images. (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) Comparison of tortuosity in control and SC patients (error bars are standard deviations).
Fig. 2
Fig. 2 Comparison of mean diameter of blood vessels in control and SC patients (superficial layer).
Fig. 3
Fig. 3 (a) Vessel perimeter map, (b) Comparison of VPI in control and SCD patients (superficial layer).
Fig. 4
Fig. 4 (a) OCTA image with demarcation for normal eye, (b) Segmented Avascular region for normal eye (c) FAZ contour for normal eye, (d) OCTA image with demarcation for diseased eye, (e) Segmented avascular region for diseased eye, (f) FAZ contour for diseased eye, (g) Comparison of area of FAZ in control and SCD patients for deep and superficial layers, (h) Comparison of area of FAZ in control and SCD patients for deep and superficial layers.
Fig. 5
Fig. 5 Contour maps created with normalized values of local fractal dimension. (a) Circular zones of diameter 1, 2 and 3mm, (b) Nasal, Superior, Temporal and Inferior regions. FD analysis was conducted on the different regions specified in a and b.
Fig. 6
Fig. 6 Comparison of vascular density in different sections of the OCTA image in control and patient eyes. Control eye: (a) Avascular region density, (b) Vessel density, (c) Grey zone density; Patient eye: (d) Avascular region density, (e) Vessel density, (f) Grey zone density.

Tables (2)

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Table 1 Vascular density changes in different zones

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Table 2 Quantitative comparison of parameters

Equations (8)

Equations on this page are rendered with MathJax. Learn more.

Euclidean distance=  ( x 1 x 2 ) 2 + ( y 1 y 2 ) 2 .
Geodesic distance=  t 0 t 1   ( dx( t ) dt ) 2  +  ( dy( t ) dt ) 2  dt.
Tortuosity= 1 n i=1 n ( Geodesic distance between two endpoints of a vessel branch i Euclidean distance between two endpoints of a vessel branch i ).
Mean vessel width= i=1,j=1 n B( i,j )  i=1,j=1 n S( i,j )  .
Vessel perimeter index= i=1,j=1 n P( i,j )  i=1,j=1 n I( i,j )  .
FAZ=(Area of single pixel( in µ m 2 )× i=1,j=1 n A( i,j ).
Contour irregularity= i=1,j=1 n O( i,j )  i=1,j=1 n R( i,j )  .
q( i,j )=LFD[p( i+k,j+k ); w<k<w].

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