Abstract

The choriocapillaris is a unique vascular plexus located posterior to the retinal pigment epithelium. In recent years, there is an increasing interest in the examination of the interrelationship between the choriocapillaris and eye diseases. We used several techniques to study choroidal perfusion, including laser Doppler flowmetry, laser speckle flowgraphy, and optical coherence tomography angiography (OCTA), but with the latter no standardized algorithm for quantitative analysis has been provided. We analyzed different algorithms to quantify flow voids in non-human primates that can be easily implemented into clinical research. In-vivo, high-resolution images of the non-human primate choriocapillaris were acquired with a swept-source OCTA (SS-OCTA) system with 100kHz A-scan/s rate, over regions of 3 × 3 mm2 and 12 × 12 mm2. The areas of non-perfusion, also called flow voids, were segmented with a structural, intensity adjusted, uneven illuminance-compensated algorithm and the new technique was compared to previously published methods. The new algorithm shows improved reproducibility and may have applications in a wide array of eye diseases including age-related macular degeneration (AMD).

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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2018 (6)

E. Borrelli, E. H. Souied, K. B. Freund, G. Querques, A. Miere, O. Gal-Or, R. Sacconi, S. R. Sadda, and D. Sarraf, “Reduced choriocapillaris flow in eyes with type 3 neovascularization and age- related macular degeneration,” Retina 38(10), 1968–1976 (2018).
[Crossref] [PubMed]

Q. Zhang, F. Zheng, E. H. Motulsky, G. Gregori, Z. Chu, C. L. Chen, C. Li, L. de Sisternes, M. Durbin, P. J. Rosenfeld, and R. K. Wang, “A novel strategy for quantifying choriocapillaris flow voids using swept-source OCT angiography,” Invest. Ophthalmol. Vis. Sci. 59(1), 203–211 (2018).
[Crossref] [PubMed]

G. Calzetti, K. Fondi, A. M. Bata, N. Luft, P. A. Wozniak, K. J. Witkowska, M. Bolz, A. Popa-Cherecheanu, R. M. Werkmeister, D. Schmidl, G. Garhöfer, and L. Schmetterer, “Assessment of choroidal blood flow using laser speckle flowgraphy,” Br. J. Ophthalmol. 102(12), 1679–1683 (2018).
[PubMed]

A. C. S. Tan, G. S. Tan, A. K. Denniston, P. A. Keane, M. Ang, D. Milea, U. Chakravarthy, and C. M. G. Cheung, “An overview of the clinical applications of optical coherence tomography angiography,” Eye (Lond.) 32(2), 262–286 (2018).
[Crossref] [PubMed]

M. Ang, A. C. S. Tan, C. M. G. Cheung, P. A. Keane, R. Dolz-Marco, C. C. A. Sng, and L. Schmetterer, “Optical coherence tomography angiography: a review of current and future clinical applications,” Graefes Arch. Clin. Exp. Ophthalmol. 256(2), 237–245 (2018).
[Crossref] [PubMed]

B. Tan, B. MacLellan, E. Mason, and K. Bizheva, “Structural, functional and blood perfusion changes in the rat retina associated with elevated intraocular pressure, measured simultaneously with a combined OCT+ERG system,” PLoS One 13(3), e0193592 (2018).
[Crossref] [PubMed]

2017 (13)

A. H. Kashani, C.-L. Chen, J. K. Gahm, F. Zheng, G. M. Richter, P. J. Rosenfeld, Y. Shi, and R. K. Wang, “Optical coherence tomography angiography: A comprehensive review of current methods and clinical applications,” Prog. Retin. Eye Res. 60, 66–100 (2017).
[Crossref] [PubMed]

R. A. Linsenmeier and H. F. Zhang, “Retinal oxygen: from animals to humans,” Prog. Retin. Eye Res. 58, 115–151 (2017).
[Crossref] [PubMed]

M. Al-Sheikh, N. Phasukkijwatana, R. Dolz-Marco, M. Rahimi, N. A. Iafe, K. B. Freund, S. R. Sadda, and D. Sarraf, “Quantitative OCT angiography of the retinal microvasculature and the choriocapillaris in myopic eyes,” Invest. Ophthalmol. Vis. Sci. 58(4), 2063–2069 (2017).
[Crossref] [PubMed]

A. Uji, S. Balasubramanian, J. Lei, E. Baghdasaryan, M. Al-Sheikh, and S. R. Sadda, “Choriocapillaris Imaging Using Multiple En Face Optical Coherence Tomography Angiography Image Averaging,” JAMA Ophthalmol. 135(11), 1197–1204 (2017).
[Crossref] [PubMed]

G. Montesano, D. Allegrini, L. Colombo, L. M. Rossetti, and A. Pece, “Features of the normal choriocapillaris with OCT-angiography: Density estimation and textural properties,” PLoS One 12(10), e0185256 (2017).
[Crossref] [PubMed]

P. L. Nesper, B. T. Soetikno, and A. A. Fawzi, “Choriocapillaris nonperfusion is associated with poor visual acuity in eyes with reticular pseudodrusen,” Am. J. Ophthalmol. 174, 42–55 (2017).
[Crossref] [PubMed]

E. Borrelli, A. Uji, D. Sarraf, and S. R. Sadda, “Alterations in the choriocapillaris in intermediate age-related macular degeneration,” Invest. Ophthalmol. Vis. Sci. 58(11), 4792–4798 (2017).
[Crossref] [PubMed]

M. Nicolò, R. Rosa, D. Musetti, M. Musolino, M. Saccheggiani, and C. E. Traverso, “Choroidal vascular flow area in central serous chorioretinopathy using swept-source optical coherence tomography angiography,” Invest. Ophthalmol. Vis. Sci. 58(4), 2002–2010 (2017).
[Crossref] [PubMed]

P. L. Nesper, P. K. Roberts, A. C. Onishi, H. Chai, L. Liu, L. M. Jampol, and A. A. Fawzi, “Quantifying microvascular abnormalities with increasing severity of diabetic retinopathy using optical coherence tomography angiography,” Invest. Ophthalmol. Vis. Sci. 58(6), BIO307 (2017).
[Crossref] [PubMed]

P. L. Nesper, B. T. Soetikno, and A. A. Fawzi, “Choriocapillaris nonperfusion is associated with poor visual acuity in eyes with reticular pseudodrusen,” Am. J. Ophthalmol. 174, 42–55 (2017).
[Crossref] [PubMed]

R. F. Spaide, “Choriocapillaris signal voids in maternally inherited diabetes and deafness and in pseudoxanthoma elasticum,” Retina 37(11), 2008–2014 (2017).
[Crossref] [PubMed]

C.-L. Chen and R. K. Wang, “Optical coherence tomography based angiography [Invited],” Biomed. Opt. Express 8(2), 1056–1082 (2017).
[Crossref] [PubMed]

K. Kurokawa, Z. Liu, and D. T. Miller, “Adaptive optics optical coherence tomography angiography for morphometric analysis of choriocapillaris [Invited],” Biomed. Opt. Express 8(3), 1803–1822 (2017).
[Crossref] [PubMed]

2016 (4)

R. F. Spaide, “Choriocapillaris flow features follow a power law distribution: implications for characterization and mechanisms of disease progression,” Am. J. Ophthalmol. 170, 58–67 (2016).
[Crossref] [PubMed]

M. A. Zouache, I. Eames, C. A. Klettner, and P. J. Luthert, “Form, shape and function: segmented blood flow in the choriocapillaris,” Sci. Rep. 6(1), 35754 (2016).
[Crossref] [PubMed]

F. Alten, P. Heiduschka, C. R. Clemens, and N. Eter, “Exploring choriocapillaris under reticular pseudodrusen using OCT-Angiography,” Graefes Arch. Clin. Exp. Ophthalmol. 254(11), 2165–2173 (2016).
[Crossref] [PubMed]

T. K. Koo and M. Y. Li, “A guideline of selecting and reporting intraclass correlation coefficients for reliability research,” J. Chiropr. Med. 15(2), 155–163 (2016).
[Crossref] [PubMed]

2015 (1)

W. Choi, E. M. Moult, N. K. Waheed, M. Adhi, B. Lee, C. D. Lu, T. E. de Carlo, V. Jayaraman, P. J. Rosenfeld, J. S. Duker, and J. G. Fujimoto, “Ultrahigh-speed, swept-source optical coherence tomography angiography in nonexudative age-related macular degeneration with geographic atrophy,” Ophthalmology 122(12), 2532–2544 (2015).
[Crossref] [PubMed]

2014 (2)

R. A. Leitgeb, R. M. Werkmeister, C. Blatter, and L. Schmetterer, “Doppler optical coherence tomography,” Prog. Retin. Eye Res. 41, 26–43 (2014).
[Crossref] [PubMed]

M. Adhi, J. J. Liu, A. H. Qavi, I. Grulkowski, C. D. Lu, K. J. Mohler, D. Ferrara, M. F. Kraus, C. R. Baumal, A. J. Witkin, N. K. Waheed, J. Hornegger, J. G. Fujimoto, and J. S. Duker, “Choroidal analysis in healthy eyes using swept-source optical coherence tomography compared to spectral domain optical coherence tomography,” Am. J. Ophthalmol. 157(6), 1272–1281 (2014).
[Crossref] [PubMed]

2013 (2)

J. M. Ruiz-Moreno, I. Flores-Moreno, F. Lugo, J. Ruiz-Medrano, J. A. Montero, and M. Akiba, “Macular choroidal thickness in normal pediatric population measured by swept-source optical coherence tomography,” Invest. Ophthalmol. Vis. Sci. 54(1), 353–359 (2013).
[Crossref] [PubMed]

S. Goverdhan, H. Thomson, and A. Lotery, “Animal models of age-related macular degeneration,” Drug Discov. Today Dis. Models 10(4), e181–e187 (2013).
[Crossref]

2012 (1)

M. E. Pennesi, M. Neuringer, and R. J. Courtney, “Animal models of age related macular degeneration,” Mol. Aspects Med. 33(4), 487–509 (2012).
[Crossref] [PubMed]

2011 (3)

L. An, T. T. Shen, and R. K. Wang, “Using ultrahigh sensitive optical microangiography to achieve comprehensive depth resolved microvasculature mapping for human retina,” J. Biomed. Opt. 16(10), 106013 (2011).
[Crossref] [PubMed]

M. Hirata, A. Tsujikawa, A. Matsumoto, M. Hangai, S. Ooto, K. Yamashiro, M. Akiba, and N. Yoshimura, “Macular choroidal thickness and volume in normal subjects measured by swept-source optical coherence tomography,” Invest. Ophthalmol. Vis. Sci. 52(8), 4971–4978 (2011).
[Crossref] [PubMed]

I. Stalmans, E. Vandewalle, D. R. Anderson, V. P. Costa, R. E. P. Frenkel, G. Garhofer, J. Grunwald, K. Gugleta, A. Harris, C. Hudson, I. Januleviciene, L. Kagemann, H. Kergoat, J. V. Lovasik, I. Lanzl, A. Martinez, Q. D. Nguyen, N. Plange, H. A. Reitsamer, M. Sehi, B. Siesky, O. Zeitz, S. Orgül, and L. Schmetterer, “Use of colour Doppler imaging in ocular blood flow research,” Acta Ophthalmol. 89(8), e609–e630 (2011).
[Crossref] [PubMed]

2010 (4)

T. Sugiyama, M. Araie, C. E. Riva, L. Schmetterer, and S. Orgul, “Use of laser speckle flowgraphy in ocular blood flow research,” Acta Ophthalmol. 88(7), 723–729 (2010).
[Crossref] [PubMed]

A. Boltz, A. Luksch, B. Wimpissinger, N. Maar, G. Weigert, S. Frantal, W. Brannath, G. Garhöfer, E. Ergun, M. Stur, and L. Schmetterer, “Choroidal blood flow and progression of age-related macular degeneration in the fellow eye in patients with unilateral choroidal neovascularization,” Invest. Ophthalmol. Vis. Sci. 51(8), 4220–4225 (2010).
[Crossref] [PubMed]

R. K. Wang, L. An, P. Francis, and D. J. Wilson, “Depth-resolved imaging of capillary networks in retina and choroid using ultrahigh sensitive optical microangiography,” Opt. Lett. 35(9), 1467–1469 (2010).
[Crossref] [PubMed]

B. Potsaid, B. Baumann, D. Huang, S. Barry, A. E. Cable, J. S. Schuman, J. S. Duker, and J. G. Fujimoto, “Ultrahigh speed 1050nm swept source/Fourier domain OCT retinal and anterior segment imaging at 100,000 to 400,000 axial scans per second,” Opt. Express 18(19), 20029–20048 (2010).
[Crossref] [PubMed]

2009 (1)

Y. Chen, D. L. Burnes, M. de Bruin, M. Mujat, and J. F. de Boer, “Three-dimensional pointwise comparison of human retinal optical property at 845 and 1060 nm using optical frequency domain imaging,” J. Biomed. Opt. 14(2), 024016 (2009).
[Crossref] [PubMed]

2008 (1)

T. I. Metelitsina, J. E. Grunwald, J. C. DuPont, G. S. Ying, A. J. Brucker, and J. L. Dunaief, “Foveolar choroidal circulation and choroidal neovascularization in age-related macular degeneration,” Invest. Ophthalmol. Vis. Sci. 49(1), 358–363 (2008).
[Crossref] [PubMed]

1994 (3)

C. E. Riva, S. D. Cranstoun, J. E. Grunwald, and B. L. Petrig, “Choroidal blood flow in the foveal region of the human ocular fundus,” Invest. Ophthalmol. Vis. Sci. 35(13), 4273–4281 (1994).
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D. S. McLeod and G. A. Lutty, “High-resolution histologic analysis of the human choroidal vasculature,” Invest. Ophthalmol. Vis. Sci. 35(11), 3799–3811 (1994).
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R. S. Ramrattan, T. L. van der Schaft, C. M. Mooy, W. C. de Bruijn, P. G. H. Mulder, and P. T. V. M. de Jong, “Morphometric analysis of Bruch’s membrane, the choriocapillaris, and the choroid in aging,” Invest. Ophthalmol. Vis. Sci. 35(6), 2857–2864 (1994).
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1992 (1)

J. B. Jonas, U. Schneider, and G. O. H. Naumann, “Count and density of human retinal photoreceptors,” Graefes Arch. Clin. Exp. Ophthalmol. 230(6), 505–510 (1992).
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1990 (1)

J. M. Olver, “Functional anatomy of the choroidal circulation: methyl methacrylate casting of human choroid,” Eye (Lond.) 4(Pt 2), 262–272 (1990).
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1979 (1)

N. Otsu, “A threshold selection method from gray-level histograms,” IEEE Trans. Syst. Man Cybern. 9(1), 62–66 (1979).
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Adhi, M.

W. Choi, E. M. Moult, N. K. Waheed, M. Adhi, B. Lee, C. D. Lu, T. E. de Carlo, V. Jayaraman, P. J. Rosenfeld, J. S. Duker, and J. G. Fujimoto, “Ultrahigh-speed, swept-source optical coherence tomography angiography in nonexudative age-related macular degeneration with geographic atrophy,” Ophthalmology 122(12), 2532–2544 (2015).
[Crossref] [PubMed]

M. Adhi, J. J. Liu, A. H. Qavi, I. Grulkowski, C. D. Lu, K. J. Mohler, D. Ferrara, M. F. Kraus, C. R. Baumal, A. J. Witkin, N. K. Waheed, J. Hornegger, J. G. Fujimoto, and J. S. Duker, “Choroidal analysis in healthy eyes using swept-source optical coherence tomography compared to spectral domain optical coherence tomography,” Am. J. Ophthalmol. 157(6), 1272–1281 (2014).
[Crossref] [PubMed]

Akiba, M.

J. M. Ruiz-Moreno, I. Flores-Moreno, F. Lugo, J. Ruiz-Medrano, J. A. Montero, and M. Akiba, “Macular choroidal thickness in normal pediatric population measured by swept-source optical coherence tomography,” Invest. Ophthalmol. Vis. Sci. 54(1), 353–359 (2013).
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M. Hirata, A. Tsujikawa, A. Matsumoto, M. Hangai, S. Ooto, K. Yamashiro, M. Akiba, and N. Yoshimura, “Macular choroidal thickness and volume in normal subjects measured by swept-source optical coherence tomography,” Invest. Ophthalmol. Vis. Sci. 52(8), 4971–4978 (2011).
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Allegrini, D.

G. Montesano, D. Allegrini, L. Colombo, L. M. Rossetti, and A. Pece, “Features of the normal choriocapillaris with OCT-angiography: Density estimation and textural properties,” PLoS One 12(10), e0185256 (2017).
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Al-Sheikh, M.

A. Uji, S. Balasubramanian, J. Lei, E. Baghdasaryan, M. Al-Sheikh, and S. R. Sadda, “Choriocapillaris Imaging Using Multiple En Face Optical Coherence Tomography Angiography Image Averaging,” JAMA Ophthalmol. 135(11), 1197–1204 (2017).
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M. Al-Sheikh, N. Phasukkijwatana, R. Dolz-Marco, M. Rahimi, N. A. Iafe, K. B. Freund, S. R. Sadda, and D. Sarraf, “Quantitative OCT angiography of the retinal microvasculature and the choriocapillaris in myopic eyes,” Invest. Ophthalmol. Vis. Sci. 58(4), 2063–2069 (2017).
[Crossref] [PubMed]

Alten, F.

F. Alten, P. Heiduschka, C. R. Clemens, and N. Eter, “Exploring choriocapillaris under reticular pseudodrusen using OCT-Angiography,” Graefes Arch. Clin. Exp. Ophthalmol. 254(11), 2165–2173 (2016).
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An, L.

L. An, T. T. Shen, and R. K. Wang, “Using ultrahigh sensitive optical microangiography to achieve comprehensive depth resolved microvasculature mapping for human retina,” J. Biomed. Opt. 16(10), 106013 (2011).
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R. K. Wang, L. An, P. Francis, and D. J. Wilson, “Depth-resolved imaging of capillary networks in retina and choroid using ultrahigh sensitive optical microangiography,” Opt. Lett. 35(9), 1467–1469 (2010).
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Anderson, D. R.

I. Stalmans, E. Vandewalle, D. R. Anderson, V. P. Costa, R. E. P. Frenkel, G. Garhofer, J. Grunwald, K. Gugleta, A. Harris, C. Hudson, I. Januleviciene, L. Kagemann, H. Kergoat, J. V. Lovasik, I. Lanzl, A. Martinez, Q. D. Nguyen, N. Plange, H. A. Reitsamer, M. Sehi, B. Siesky, O. Zeitz, S. Orgül, and L. Schmetterer, “Use of colour Doppler imaging in ocular blood flow research,” Acta Ophthalmol. 89(8), e609–e630 (2011).
[Crossref] [PubMed]

Ang, M.

A. C. S. Tan, G. S. Tan, A. K. Denniston, P. A. Keane, M. Ang, D. Milea, U. Chakravarthy, and C. M. G. Cheung, “An overview of the clinical applications of optical coherence tomography angiography,” Eye (Lond.) 32(2), 262–286 (2018).
[Crossref] [PubMed]

M. Ang, A. C. S. Tan, C. M. G. Cheung, P. A. Keane, R. Dolz-Marco, C. C. A. Sng, and L. Schmetterer, “Optical coherence tomography angiography: a review of current and future clinical applications,” Graefes Arch. Clin. Exp. Ophthalmol. 256(2), 237–245 (2018).
[Crossref] [PubMed]

Araie, M.

T. Sugiyama, M. Araie, C. E. Riva, L. Schmetterer, and S. Orgul, “Use of laser speckle flowgraphy in ocular blood flow research,” Acta Ophthalmol. 88(7), 723–729 (2010).
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Baghdasaryan, E.

A. Uji, S. Balasubramanian, J. Lei, E. Baghdasaryan, M. Al-Sheikh, and S. R. Sadda, “Choriocapillaris Imaging Using Multiple En Face Optical Coherence Tomography Angiography Image Averaging,” JAMA Ophthalmol. 135(11), 1197–1204 (2017).
[Crossref] [PubMed]

Balasubramanian, S.

A. Uji, S. Balasubramanian, J. Lei, E. Baghdasaryan, M. Al-Sheikh, and S. R. Sadda, “Choriocapillaris Imaging Using Multiple En Face Optical Coherence Tomography Angiography Image Averaging,” JAMA Ophthalmol. 135(11), 1197–1204 (2017).
[Crossref] [PubMed]

Barry, S.

Bata, A. M.

G. Calzetti, K. Fondi, A. M. Bata, N. Luft, P. A. Wozniak, K. J. Witkowska, M. Bolz, A. Popa-Cherecheanu, R. M. Werkmeister, D. Schmidl, G. Garhöfer, and L. Schmetterer, “Assessment of choroidal blood flow using laser speckle flowgraphy,” Br. J. Ophthalmol. 102(12), 1679–1683 (2018).
[PubMed]

Baumal, C. R.

M. Adhi, J. J. Liu, A. H. Qavi, I. Grulkowski, C. D. Lu, K. J. Mohler, D. Ferrara, M. F. Kraus, C. R. Baumal, A. J. Witkin, N. K. Waheed, J. Hornegger, J. G. Fujimoto, and J. S. Duker, “Choroidal analysis in healthy eyes using swept-source optical coherence tomography compared to spectral domain optical coherence tomography,” Am. J. Ophthalmol. 157(6), 1272–1281 (2014).
[Crossref] [PubMed]

Baumann, B.

Bizheva, K.

B. Tan, B. MacLellan, E. Mason, and K. Bizheva, “Structural, functional and blood perfusion changes in the rat retina associated with elevated intraocular pressure, measured simultaneously with a combined OCT+ERG system,” PLoS One 13(3), e0193592 (2018).
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Blatter, C.

R. A. Leitgeb, R. M. Werkmeister, C. Blatter, and L. Schmetterer, “Doppler optical coherence tomography,” Prog. Retin. Eye Res. 41, 26–43 (2014).
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Boltz, A.

A. Boltz, A. Luksch, B. Wimpissinger, N. Maar, G. Weigert, S. Frantal, W. Brannath, G. Garhöfer, E. Ergun, M. Stur, and L. Schmetterer, “Choroidal blood flow and progression of age-related macular degeneration in the fellow eye in patients with unilateral choroidal neovascularization,” Invest. Ophthalmol. Vis. Sci. 51(8), 4220–4225 (2010).
[Crossref] [PubMed]

Bolz, M.

G. Calzetti, K. Fondi, A. M. Bata, N. Luft, P. A. Wozniak, K. J. Witkowska, M. Bolz, A. Popa-Cherecheanu, R. M. Werkmeister, D. Schmidl, G. Garhöfer, and L. Schmetterer, “Assessment of choroidal blood flow using laser speckle flowgraphy,” Br. J. Ophthalmol. 102(12), 1679–1683 (2018).
[PubMed]

Borrelli, E.

E. Borrelli, E. H. Souied, K. B. Freund, G. Querques, A. Miere, O. Gal-Or, R. Sacconi, S. R. Sadda, and D. Sarraf, “Reduced choriocapillaris flow in eyes with type 3 neovascularization and age- related macular degeneration,” Retina 38(10), 1968–1976 (2018).
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E. Borrelli, A. Uji, D. Sarraf, and S. R. Sadda, “Alterations in the choriocapillaris in intermediate age-related macular degeneration,” Invest. Ophthalmol. Vis. Sci. 58(11), 4792–4798 (2017).
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Brannath, W.

A. Boltz, A. Luksch, B. Wimpissinger, N. Maar, G. Weigert, S. Frantal, W. Brannath, G. Garhöfer, E. Ergun, M. Stur, and L. Schmetterer, “Choroidal blood flow and progression of age-related macular degeneration in the fellow eye in patients with unilateral choroidal neovascularization,” Invest. Ophthalmol. Vis. Sci. 51(8), 4220–4225 (2010).
[Crossref] [PubMed]

Brucker, A. J.

T. I. Metelitsina, J. E. Grunwald, J. C. DuPont, G. S. Ying, A. J. Brucker, and J. L. Dunaief, “Foveolar choroidal circulation and choroidal neovascularization in age-related macular degeneration,” Invest. Ophthalmol. Vis. Sci. 49(1), 358–363 (2008).
[Crossref] [PubMed]

Burnes, D. L.

Y. Chen, D. L. Burnes, M. de Bruin, M. Mujat, and J. F. de Boer, “Three-dimensional pointwise comparison of human retinal optical property at 845 and 1060 nm using optical frequency domain imaging,” J. Biomed. Opt. 14(2), 024016 (2009).
[Crossref] [PubMed]

Cable, A. E.

Calzetti, G.

G. Calzetti, K. Fondi, A. M. Bata, N. Luft, P. A. Wozniak, K. J. Witkowska, M. Bolz, A. Popa-Cherecheanu, R. M. Werkmeister, D. Schmidl, G. Garhöfer, and L. Schmetterer, “Assessment of choroidal blood flow using laser speckle flowgraphy,” Br. J. Ophthalmol. 102(12), 1679–1683 (2018).
[PubMed]

Chai, H.

P. L. Nesper, P. K. Roberts, A. C. Onishi, H. Chai, L. Liu, L. M. Jampol, and A. A. Fawzi, “Quantifying microvascular abnormalities with increasing severity of diabetic retinopathy using optical coherence tomography angiography,” Invest. Ophthalmol. Vis. Sci. 58(6), BIO307 (2017).
[Crossref] [PubMed]

Chakravarthy, U.

A. C. S. Tan, G. S. Tan, A. K. Denniston, P. A. Keane, M. Ang, D. Milea, U. Chakravarthy, and C. M. G. Cheung, “An overview of the clinical applications of optical coherence tomography angiography,” Eye (Lond.) 32(2), 262–286 (2018).
[Crossref] [PubMed]

Chen, C. L.

Q. Zhang, F. Zheng, E. H. Motulsky, G. Gregori, Z. Chu, C. L. Chen, C. Li, L. de Sisternes, M. Durbin, P. J. Rosenfeld, and R. K. Wang, “A novel strategy for quantifying choriocapillaris flow voids using swept-source OCT angiography,” Invest. Ophthalmol. Vis. Sci. 59(1), 203–211 (2018).
[Crossref] [PubMed]

Chen, C.-L.

A. H. Kashani, C.-L. Chen, J. K. Gahm, F. Zheng, G. M. Richter, P. J. Rosenfeld, Y. Shi, and R. K. Wang, “Optical coherence tomography angiography: A comprehensive review of current methods and clinical applications,” Prog. Retin. Eye Res. 60, 66–100 (2017).
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C.-L. Chen and R. K. Wang, “Optical coherence tomography based angiography [Invited],” Biomed. Opt. Express 8(2), 1056–1082 (2017).
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Chen, Y.

Y. Chen, D. L. Burnes, M. de Bruin, M. Mujat, and J. F. de Boer, “Three-dimensional pointwise comparison of human retinal optical property at 845 and 1060 nm using optical frequency domain imaging,” J. Biomed. Opt. 14(2), 024016 (2009).
[Crossref] [PubMed]

Cheung, C. M. G.

A. C. S. Tan, G. S. Tan, A. K. Denniston, P. A. Keane, M. Ang, D. Milea, U. Chakravarthy, and C. M. G. Cheung, “An overview of the clinical applications of optical coherence tomography angiography,” Eye (Lond.) 32(2), 262–286 (2018).
[Crossref] [PubMed]

M. Ang, A. C. S. Tan, C. M. G. Cheung, P. A. Keane, R. Dolz-Marco, C. C. A. Sng, and L. Schmetterer, “Optical coherence tomography angiography: a review of current and future clinical applications,” Graefes Arch. Clin. Exp. Ophthalmol. 256(2), 237–245 (2018).
[Crossref] [PubMed]

Choi, W.

W. Choi, E. M. Moult, N. K. Waheed, M. Adhi, B. Lee, C. D. Lu, T. E. de Carlo, V. Jayaraman, P. J. Rosenfeld, J. S. Duker, and J. G. Fujimoto, “Ultrahigh-speed, swept-source optical coherence tomography angiography in nonexudative age-related macular degeneration with geographic atrophy,” Ophthalmology 122(12), 2532–2544 (2015).
[Crossref] [PubMed]

Chu, Z.

Q. Zhang, F. Zheng, E. H. Motulsky, G. Gregori, Z. Chu, C. L. Chen, C. Li, L. de Sisternes, M. Durbin, P. J. Rosenfeld, and R. K. Wang, “A novel strategy for quantifying choriocapillaris flow voids using swept-source OCT angiography,” Invest. Ophthalmol. Vis. Sci. 59(1), 203–211 (2018).
[Crossref] [PubMed]

Clemens, C. R.

F. Alten, P. Heiduschka, C. R. Clemens, and N. Eter, “Exploring choriocapillaris under reticular pseudodrusen using OCT-Angiography,” Graefes Arch. Clin. Exp. Ophthalmol. 254(11), 2165–2173 (2016).
[Crossref] [PubMed]

Colombo, L.

G. Montesano, D. Allegrini, L. Colombo, L. M. Rossetti, and A. Pece, “Features of the normal choriocapillaris with OCT-angiography: Density estimation and textural properties,” PLoS One 12(10), e0185256 (2017).
[Crossref] [PubMed]

Costa, V. P.

I. Stalmans, E. Vandewalle, D. R. Anderson, V. P. Costa, R. E. P. Frenkel, G. Garhofer, J. Grunwald, K. Gugleta, A. Harris, C. Hudson, I. Januleviciene, L. Kagemann, H. Kergoat, J. V. Lovasik, I. Lanzl, A. Martinez, Q. D. Nguyen, N. Plange, H. A. Reitsamer, M. Sehi, B. Siesky, O. Zeitz, S. Orgül, and L. Schmetterer, “Use of colour Doppler imaging in ocular blood flow research,” Acta Ophthalmol. 89(8), e609–e630 (2011).
[Crossref] [PubMed]

Courtney, R. J.

M. E. Pennesi, M. Neuringer, and R. J. Courtney, “Animal models of age related macular degeneration,” Mol. Aspects Med. 33(4), 487–509 (2012).
[Crossref] [PubMed]

Cranstoun, S. D.

C. E. Riva, S. D. Cranstoun, J. E. Grunwald, and B. L. Petrig, “Choroidal blood flow in the foveal region of the human ocular fundus,” Invest. Ophthalmol. Vis. Sci. 35(13), 4273–4281 (1994).
[PubMed]

de Boer, J. F.

Y. Chen, D. L. Burnes, M. de Bruin, M. Mujat, and J. F. de Boer, “Three-dimensional pointwise comparison of human retinal optical property at 845 and 1060 nm using optical frequency domain imaging,” J. Biomed. Opt. 14(2), 024016 (2009).
[Crossref] [PubMed]

de Bruijn, W. C.

R. S. Ramrattan, T. L. van der Schaft, C. M. Mooy, W. C. de Bruijn, P. G. H. Mulder, and P. T. V. M. de Jong, “Morphometric analysis of Bruch’s membrane, the choriocapillaris, and the choroid in aging,” Invest. Ophthalmol. Vis. Sci. 35(6), 2857–2864 (1994).
[PubMed]

de Bruin, M.

Y. Chen, D. L. Burnes, M. de Bruin, M. Mujat, and J. F. de Boer, “Three-dimensional pointwise comparison of human retinal optical property at 845 and 1060 nm using optical frequency domain imaging,” J. Biomed. Opt. 14(2), 024016 (2009).
[Crossref] [PubMed]

de Carlo, T. E.

W. Choi, E. M. Moult, N. K. Waheed, M. Adhi, B. Lee, C. D. Lu, T. E. de Carlo, V. Jayaraman, P. J. Rosenfeld, J. S. Duker, and J. G. Fujimoto, “Ultrahigh-speed, swept-source optical coherence tomography angiography in nonexudative age-related macular degeneration with geographic atrophy,” Ophthalmology 122(12), 2532–2544 (2015).
[Crossref] [PubMed]

de Jong, P. T. V. M.

R. S. Ramrattan, T. L. van der Schaft, C. M. Mooy, W. C. de Bruijn, P. G. H. Mulder, and P. T. V. M. de Jong, “Morphometric analysis of Bruch’s membrane, the choriocapillaris, and the choroid in aging,” Invest. Ophthalmol. Vis. Sci. 35(6), 2857–2864 (1994).
[PubMed]

de Sisternes, L.

Q. Zhang, F. Zheng, E. H. Motulsky, G. Gregori, Z. Chu, C. L. Chen, C. Li, L. de Sisternes, M. Durbin, P. J. Rosenfeld, and R. K. Wang, “A novel strategy for quantifying choriocapillaris flow voids using swept-source OCT angiography,” Invest. Ophthalmol. Vis. Sci. 59(1), 203–211 (2018).
[Crossref] [PubMed]

Denniston, A. K.

A. C. S. Tan, G. S. Tan, A. K. Denniston, P. A. Keane, M. Ang, D. Milea, U. Chakravarthy, and C. M. G. Cheung, “An overview of the clinical applications of optical coherence tomography angiography,” Eye (Lond.) 32(2), 262–286 (2018).
[Crossref] [PubMed]

Dolz-Marco, R.

M. Ang, A. C. S. Tan, C. M. G. Cheung, P. A. Keane, R. Dolz-Marco, C. C. A. Sng, and L. Schmetterer, “Optical coherence tomography angiography: a review of current and future clinical applications,” Graefes Arch. Clin. Exp. Ophthalmol. 256(2), 237–245 (2018).
[Crossref] [PubMed]

M. Al-Sheikh, N. Phasukkijwatana, R. Dolz-Marco, M. Rahimi, N. A. Iafe, K. B. Freund, S. R. Sadda, and D. Sarraf, “Quantitative OCT angiography of the retinal microvasculature and the choriocapillaris in myopic eyes,” Invest. Ophthalmol. Vis. Sci. 58(4), 2063–2069 (2017).
[Crossref] [PubMed]

Duker, J. S.

W. Choi, E. M. Moult, N. K. Waheed, M. Adhi, B. Lee, C. D. Lu, T. E. de Carlo, V. Jayaraman, P. J. Rosenfeld, J. S. Duker, and J. G. Fujimoto, “Ultrahigh-speed, swept-source optical coherence tomography angiography in nonexudative age-related macular degeneration with geographic atrophy,” Ophthalmology 122(12), 2532–2544 (2015).
[Crossref] [PubMed]

M. Adhi, J. J. Liu, A. H. Qavi, I. Grulkowski, C. D. Lu, K. J. Mohler, D. Ferrara, M. F. Kraus, C. R. Baumal, A. J. Witkin, N. K. Waheed, J. Hornegger, J. G. Fujimoto, and J. S. Duker, “Choroidal analysis in healthy eyes using swept-source optical coherence tomography compared to spectral domain optical coherence tomography,” Am. J. Ophthalmol. 157(6), 1272–1281 (2014).
[Crossref] [PubMed]

B. Potsaid, B. Baumann, D. Huang, S. Barry, A. E. Cable, J. S. Schuman, J. S. Duker, and J. G. Fujimoto, “Ultrahigh speed 1050nm swept source/Fourier domain OCT retinal and anterior segment imaging at 100,000 to 400,000 axial scans per second,” Opt. Express 18(19), 20029–20048 (2010).
[Crossref] [PubMed]

Dunaief, J. L.

T. I. Metelitsina, J. E. Grunwald, J. C. DuPont, G. S. Ying, A. J. Brucker, and J. L. Dunaief, “Foveolar choroidal circulation and choroidal neovascularization in age-related macular degeneration,” Invest. Ophthalmol. Vis. Sci. 49(1), 358–363 (2008).
[Crossref] [PubMed]

DuPont, J. C.

T. I. Metelitsina, J. E. Grunwald, J. C. DuPont, G. S. Ying, A. J. Brucker, and J. L. Dunaief, “Foveolar choroidal circulation and choroidal neovascularization in age-related macular degeneration,” Invest. Ophthalmol. Vis. Sci. 49(1), 358–363 (2008).
[Crossref] [PubMed]

Durbin, M.

Q. Zhang, F. Zheng, E. H. Motulsky, G. Gregori, Z. Chu, C. L. Chen, C. Li, L. de Sisternes, M. Durbin, P. J. Rosenfeld, and R. K. Wang, “A novel strategy for quantifying choriocapillaris flow voids using swept-source OCT angiography,” Invest. Ophthalmol. Vis. Sci. 59(1), 203–211 (2018).
[Crossref] [PubMed]

Eames, I.

M. A. Zouache, I. Eames, C. A. Klettner, and P. J. Luthert, “Form, shape and function: segmented blood flow in the choriocapillaris,” Sci. Rep. 6(1), 35754 (2016).
[Crossref] [PubMed]

Ergun, E.

A. Boltz, A. Luksch, B. Wimpissinger, N. Maar, G. Weigert, S. Frantal, W. Brannath, G. Garhöfer, E. Ergun, M. Stur, and L. Schmetterer, “Choroidal blood flow and progression of age-related macular degeneration in the fellow eye in patients with unilateral choroidal neovascularization,” Invest. Ophthalmol. Vis. Sci. 51(8), 4220–4225 (2010).
[Crossref] [PubMed]

Eter, N.

F. Alten, P. Heiduschka, C. R. Clemens, and N. Eter, “Exploring choriocapillaris under reticular pseudodrusen using OCT-Angiography,” Graefes Arch. Clin. Exp. Ophthalmol. 254(11), 2165–2173 (2016).
[Crossref] [PubMed]

Fawzi, A. A.

P. L. Nesper, P. K. Roberts, A. C. Onishi, H. Chai, L. Liu, L. M. Jampol, and A. A. Fawzi, “Quantifying microvascular abnormalities with increasing severity of diabetic retinopathy using optical coherence tomography angiography,” Invest. Ophthalmol. Vis. Sci. 58(6), BIO307 (2017).
[Crossref] [PubMed]

P. L. Nesper, B. T. Soetikno, and A. A. Fawzi, “Choriocapillaris nonperfusion is associated with poor visual acuity in eyes with reticular pseudodrusen,” Am. J. Ophthalmol. 174, 42–55 (2017).
[Crossref] [PubMed]

P. L. Nesper, B. T. Soetikno, and A. A. Fawzi, “Choriocapillaris nonperfusion is associated with poor visual acuity in eyes with reticular pseudodrusen,” Am. J. Ophthalmol. 174, 42–55 (2017).
[Crossref] [PubMed]

Ferrara, D.

M. Adhi, J. J. Liu, A. H. Qavi, I. Grulkowski, C. D. Lu, K. J. Mohler, D. Ferrara, M. F. Kraus, C. R. Baumal, A. J. Witkin, N. K. Waheed, J. Hornegger, J. G. Fujimoto, and J. S. Duker, “Choroidal analysis in healthy eyes using swept-source optical coherence tomography compared to spectral domain optical coherence tomography,” Am. J. Ophthalmol. 157(6), 1272–1281 (2014).
[Crossref] [PubMed]

Flores-Moreno, I.

J. M. Ruiz-Moreno, I. Flores-Moreno, F. Lugo, J. Ruiz-Medrano, J. A. Montero, and M. Akiba, “Macular choroidal thickness in normal pediatric population measured by swept-source optical coherence tomography,” Invest. Ophthalmol. Vis. Sci. 54(1), 353–359 (2013).
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Fondi, K.

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T. K. Koo and M. Y. Li, “A guideline of selecting and reporting intraclass correlation coefficients for reliability research,” J. Chiropr. Med. 15(2), 155–163 (2016).
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M. A. Zouache, I. Eames, C. A. Klettner, and P. J. Luthert, “Form, shape and function: segmented blood flow in the choriocapillaris,” Sci. Rep. 6(1), 35754 (2016).
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M. E. Pennesi, M. Neuringer, and R. J. Courtney, “Animal models of age related macular degeneration,” Mol. Aspects Med. 33(4), 487–509 (2012).
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Qavi, A. H.

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E. Borrelli, E. H. Souied, K. B. Freund, G. Querques, A. Miere, O. Gal-Or, R. Sacconi, S. R. Sadda, and D. Sarraf, “Reduced choriocapillaris flow in eyes with type 3 neovascularization and age- related macular degeneration,” Retina 38(10), 1968–1976 (2018).
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R. S. Ramrattan, T. L. van der Schaft, C. M. Mooy, W. C. de Bruijn, P. G. H. Mulder, and P. T. V. M. de Jong, “Morphometric analysis of Bruch’s membrane, the choriocapillaris, and the choroid in aging,” Invest. Ophthalmol. Vis. Sci. 35(6), 2857–2864 (1994).
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I. Stalmans, E. Vandewalle, D. R. Anderson, V. P. Costa, R. E. P. Frenkel, G. Garhofer, J. Grunwald, K. Gugleta, A. Harris, C. Hudson, I. Januleviciene, L. Kagemann, H. Kergoat, J. V. Lovasik, I. Lanzl, A. Martinez, Q. D. Nguyen, N. Plange, H. A. Reitsamer, M. Sehi, B. Siesky, O. Zeitz, S. Orgül, and L. Schmetterer, “Use of colour Doppler imaging in ocular blood flow research,” Acta Ophthalmol. 89(8), e609–e630 (2011).
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A. H. Kashani, C.-L. Chen, J. K. Gahm, F. Zheng, G. M. Richter, P. J. Rosenfeld, Y. Shi, and R. K. Wang, “Optical coherence tomography angiography: A comprehensive review of current methods and clinical applications,” Prog. Retin. Eye Res. 60, 66–100 (2017).
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T. Sugiyama, M. Araie, C. E. Riva, L. Schmetterer, and S. Orgul, “Use of laser speckle flowgraphy in ocular blood flow research,” Acta Ophthalmol. 88(7), 723–729 (2010).
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C. E. Riva, S. D. Cranstoun, J. E. Grunwald, and B. L. Petrig, “Choroidal blood flow in the foveal region of the human ocular fundus,” Invest. Ophthalmol. Vis. Sci. 35(13), 4273–4281 (1994).
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P. L. Nesper, P. K. Roberts, A. C. Onishi, H. Chai, L. Liu, L. M. Jampol, and A. A. Fawzi, “Quantifying microvascular abnormalities with increasing severity of diabetic retinopathy using optical coherence tomography angiography,” Invest. Ophthalmol. Vis. Sci. 58(6), BIO307 (2017).
[Crossref] [PubMed]

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M. Nicolò, R. Rosa, D. Musetti, M. Musolino, M. Saccheggiani, and C. E. Traverso, “Choroidal vascular flow area in central serous chorioretinopathy using swept-source optical coherence tomography angiography,” Invest. Ophthalmol. Vis. Sci. 58(4), 2002–2010 (2017).
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A. H. Kashani, C.-L. Chen, J. K. Gahm, F. Zheng, G. M. Richter, P. J. Rosenfeld, Y. Shi, and R. K. Wang, “Optical coherence tomography angiography: A comprehensive review of current methods and clinical applications,” Prog. Retin. Eye Res. 60, 66–100 (2017).
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W. Choi, E. M. Moult, N. K. Waheed, M. Adhi, B. Lee, C. D. Lu, T. E. de Carlo, V. Jayaraman, P. J. Rosenfeld, J. S. Duker, and J. G. Fujimoto, “Ultrahigh-speed, swept-source optical coherence tomography angiography in nonexudative age-related macular degeneration with geographic atrophy,” Ophthalmology 122(12), 2532–2544 (2015).
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Rossetti, L. M.

G. Montesano, D. Allegrini, L. Colombo, L. M. Rossetti, and A. Pece, “Features of the normal choriocapillaris with OCT-angiography: Density estimation and textural properties,” PLoS One 12(10), e0185256 (2017).
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J. M. Ruiz-Moreno, I. Flores-Moreno, F. Lugo, J. Ruiz-Medrano, J. A. Montero, and M. Akiba, “Macular choroidal thickness in normal pediatric population measured by swept-source optical coherence tomography,” Invest. Ophthalmol. Vis. Sci. 54(1), 353–359 (2013).
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J. M. Ruiz-Moreno, I. Flores-Moreno, F. Lugo, J. Ruiz-Medrano, J. A. Montero, and M. Akiba, “Macular choroidal thickness in normal pediatric population measured by swept-source optical coherence tomography,” Invest. Ophthalmol. Vis. Sci. 54(1), 353–359 (2013).
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Saccheggiani, M.

M. Nicolò, R. Rosa, D. Musetti, M. Musolino, M. Saccheggiani, and C. E. Traverso, “Choroidal vascular flow area in central serous chorioretinopathy using swept-source optical coherence tomography angiography,” Invest. Ophthalmol. Vis. Sci. 58(4), 2002–2010 (2017).
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E. Borrelli, E. H. Souied, K. B. Freund, G. Querques, A. Miere, O. Gal-Or, R. Sacconi, S. R. Sadda, and D. Sarraf, “Reduced choriocapillaris flow in eyes with type 3 neovascularization and age- related macular degeneration,” Retina 38(10), 1968–1976 (2018).
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Sadda, S. R.

E. Borrelli, E. H. Souied, K. B. Freund, G. Querques, A. Miere, O. Gal-Or, R. Sacconi, S. R. Sadda, and D. Sarraf, “Reduced choriocapillaris flow in eyes with type 3 neovascularization and age- related macular degeneration,” Retina 38(10), 1968–1976 (2018).
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E. Borrelli, A. Uji, D. Sarraf, and S. R. Sadda, “Alterations in the choriocapillaris in intermediate age-related macular degeneration,” Invest. Ophthalmol. Vis. Sci. 58(11), 4792–4798 (2017).
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M. Al-Sheikh, N. Phasukkijwatana, R. Dolz-Marco, M. Rahimi, N. A. Iafe, K. B. Freund, S. R. Sadda, and D. Sarraf, “Quantitative OCT angiography of the retinal microvasculature and the choriocapillaris in myopic eyes,” Invest. Ophthalmol. Vis. Sci. 58(4), 2063–2069 (2017).
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A. Uji, S. Balasubramanian, J. Lei, E. Baghdasaryan, M. Al-Sheikh, and S. R. Sadda, “Choriocapillaris Imaging Using Multiple En Face Optical Coherence Tomography Angiography Image Averaging,” JAMA Ophthalmol. 135(11), 1197–1204 (2017).
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Sarraf, D.

E. Borrelli, E. H. Souied, K. B. Freund, G. Querques, A. Miere, O. Gal-Or, R. Sacconi, S. R. Sadda, and D. Sarraf, “Reduced choriocapillaris flow in eyes with type 3 neovascularization and age- related macular degeneration,” Retina 38(10), 1968–1976 (2018).
[Crossref] [PubMed]

M. Al-Sheikh, N. Phasukkijwatana, R. Dolz-Marco, M. Rahimi, N. A. Iafe, K. B. Freund, S. R. Sadda, and D. Sarraf, “Quantitative OCT angiography of the retinal microvasculature and the choriocapillaris in myopic eyes,” Invest. Ophthalmol. Vis. Sci. 58(4), 2063–2069 (2017).
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E. Borrelli, A. Uji, D. Sarraf, and S. R. Sadda, “Alterations in the choriocapillaris in intermediate age-related macular degeneration,” Invest. Ophthalmol. Vis. Sci. 58(11), 4792–4798 (2017).
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Schmetterer, L.

G. Calzetti, K. Fondi, A. M. Bata, N. Luft, P. A. Wozniak, K. J. Witkowska, M. Bolz, A. Popa-Cherecheanu, R. M. Werkmeister, D. Schmidl, G. Garhöfer, and L. Schmetterer, “Assessment of choroidal blood flow using laser speckle flowgraphy,” Br. J. Ophthalmol. 102(12), 1679–1683 (2018).
[PubMed]

M. Ang, A. C. S. Tan, C. M. G. Cheung, P. A. Keane, R. Dolz-Marco, C. C. A. Sng, and L. Schmetterer, “Optical coherence tomography angiography: a review of current and future clinical applications,” Graefes Arch. Clin. Exp. Ophthalmol. 256(2), 237–245 (2018).
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R. A. Leitgeb, R. M. Werkmeister, C. Blatter, and L. Schmetterer, “Doppler optical coherence tomography,” Prog. Retin. Eye Res. 41, 26–43 (2014).
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I. Stalmans, E. Vandewalle, D. R. Anderson, V. P. Costa, R. E. P. Frenkel, G. Garhofer, J. Grunwald, K. Gugleta, A. Harris, C. Hudson, I. Januleviciene, L. Kagemann, H. Kergoat, J. V. Lovasik, I. Lanzl, A. Martinez, Q. D. Nguyen, N. Plange, H. A. Reitsamer, M. Sehi, B. Siesky, O. Zeitz, S. Orgül, and L. Schmetterer, “Use of colour Doppler imaging in ocular blood flow research,” Acta Ophthalmol. 89(8), e609–e630 (2011).
[Crossref] [PubMed]

T. Sugiyama, M. Araie, C. E. Riva, L. Schmetterer, and S. Orgul, “Use of laser speckle flowgraphy in ocular blood flow research,” Acta Ophthalmol. 88(7), 723–729 (2010).
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A. Boltz, A. Luksch, B. Wimpissinger, N. Maar, G. Weigert, S. Frantal, W. Brannath, G. Garhöfer, E. Ergun, M. Stur, and L. Schmetterer, “Choroidal blood flow and progression of age-related macular degeneration in the fellow eye in patients with unilateral choroidal neovascularization,” Invest. Ophthalmol. Vis. Sci. 51(8), 4220–4225 (2010).
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Schmidl, D.

G. Calzetti, K. Fondi, A. M. Bata, N. Luft, P. A. Wozniak, K. J. Witkowska, M. Bolz, A. Popa-Cherecheanu, R. M. Werkmeister, D. Schmidl, G. Garhöfer, and L. Schmetterer, “Assessment of choroidal blood flow using laser speckle flowgraphy,” Br. J. Ophthalmol. 102(12), 1679–1683 (2018).
[PubMed]

Schneider, U.

J. B. Jonas, U. Schneider, and G. O. H. Naumann, “Count and density of human retinal photoreceptors,” Graefes Arch. Clin. Exp. Ophthalmol. 230(6), 505–510 (1992).
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Schuman, J. S.

Sehi, M.

I. Stalmans, E. Vandewalle, D. R. Anderson, V. P. Costa, R. E. P. Frenkel, G. Garhofer, J. Grunwald, K. Gugleta, A. Harris, C. Hudson, I. Januleviciene, L. Kagemann, H. Kergoat, J. V. Lovasik, I. Lanzl, A. Martinez, Q. D. Nguyen, N. Plange, H. A. Reitsamer, M. Sehi, B. Siesky, O. Zeitz, S. Orgül, and L. Schmetterer, “Use of colour Doppler imaging in ocular blood flow research,” Acta Ophthalmol. 89(8), e609–e630 (2011).
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Shen, T. T.

L. An, T. T. Shen, and R. K. Wang, “Using ultrahigh sensitive optical microangiography to achieve comprehensive depth resolved microvasculature mapping for human retina,” J. Biomed. Opt. 16(10), 106013 (2011).
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Shi, Y.

A. H. Kashani, C.-L. Chen, J. K. Gahm, F. Zheng, G. M. Richter, P. J. Rosenfeld, Y. Shi, and R. K. Wang, “Optical coherence tomography angiography: A comprehensive review of current methods and clinical applications,” Prog. Retin. Eye Res. 60, 66–100 (2017).
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Siesky, B.

I. Stalmans, E. Vandewalle, D. R. Anderson, V. P. Costa, R. E. P. Frenkel, G. Garhofer, J. Grunwald, K. Gugleta, A. Harris, C. Hudson, I. Januleviciene, L. Kagemann, H. Kergoat, J. V. Lovasik, I. Lanzl, A. Martinez, Q. D. Nguyen, N. Plange, H. A. Reitsamer, M. Sehi, B. Siesky, O. Zeitz, S. Orgül, and L. Schmetterer, “Use of colour Doppler imaging in ocular blood flow research,” Acta Ophthalmol. 89(8), e609–e630 (2011).
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Sng, C. C. A.

M. Ang, A. C. S. Tan, C. M. G. Cheung, P. A. Keane, R. Dolz-Marco, C. C. A. Sng, and L. Schmetterer, “Optical coherence tomography angiography: a review of current and future clinical applications,” Graefes Arch. Clin. Exp. Ophthalmol. 256(2), 237–245 (2018).
[Crossref] [PubMed]

Soetikno, B. T.

P. L. Nesper, B. T. Soetikno, and A. A. Fawzi, “Choriocapillaris nonperfusion is associated with poor visual acuity in eyes with reticular pseudodrusen,” Am. J. Ophthalmol. 174, 42–55 (2017).
[Crossref] [PubMed]

P. L. Nesper, B. T. Soetikno, and A. A. Fawzi, “Choriocapillaris nonperfusion is associated with poor visual acuity in eyes with reticular pseudodrusen,” Am. J. Ophthalmol. 174, 42–55 (2017).
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Souied, E. H.

E. Borrelli, E. H. Souied, K. B. Freund, G. Querques, A. Miere, O. Gal-Or, R. Sacconi, S. R. Sadda, and D. Sarraf, “Reduced choriocapillaris flow in eyes with type 3 neovascularization and age- related macular degeneration,” Retina 38(10), 1968–1976 (2018).
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R. F. Spaide, “Choriocapillaris flow features follow a power law distribution: implications for characterization and mechanisms of disease progression,” Am. J. Ophthalmol. 170, 58–67 (2016).
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A. Boltz, A. Luksch, B. Wimpissinger, N. Maar, G. Weigert, S. Frantal, W. Brannath, G. Garhöfer, E. Ergun, M. Stur, and L. Schmetterer, “Choroidal blood flow and progression of age-related macular degeneration in the fellow eye in patients with unilateral choroidal neovascularization,” Invest. Ophthalmol. Vis. Sci. 51(8), 4220–4225 (2010).
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T. Sugiyama, M. Araie, C. E. Riva, L. Schmetterer, and S. Orgul, “Use of laser speckle flowgraphy in ocular blood flow research,” Acta Ophthalmol. 88(7), 723–729 (2010).
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M. Ang, A. C. S. Tan, C. M. G. Cheung, P. A. Keane, R. Dolz-Marco, C. C. A. Sng, and L. Schmetterer, “Optical coherence tomography angiography: a review of current and future clinical applications,” Graefes Arch. Clin. Exp. Ophthalmol. 256(2), 237–245 (2018).
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A. C. S. Tan, G. S. Tan, A. K. Denniston, P. A. Keane, M. Ang, D. Milea, U. Chakravarthy, and C. M. G. Cheung, “An overview of the clinical applications of optical coherence tomography angiography,” Eye (Lond.) 32(2), 262–286 (2018).
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Tan, B.

B. Tan, B. MacLellan, E. Mason, and K. Bizheva, “Structural, functional and blood perfusion changes in the rat retina associated with elevated intraocular pressure, measured simultaneously with a combined OCT+ERG system,” PLoS One 13(3), e0193592 (2018).
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A. C. S. Tan, G. S. Tan, A. K. Denniston, P. A. Keane, M. Ang, D. Milea, U. Chakravarthy, and C. M. G. Cheung, “An overview of the clinical applications of optical coherence tomography angiography,” Eye (Lond.) 32(2), 262–286 (2018).
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Thomson, H.

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M. Nicolò, R. Rosa, D. Musetti, M. Musolino, M. Saccheggiani, and C. E. Traverso, “Choroidal vascular flow area in central serous chorioretinopathy using swept-source optical coherence tomography angiography,” Invest. Ophthalmol. Vis. Sci. 58(4), 2002–2010 (2017).
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A. Uji, S. Balasubramanian, J. Lei, E. Baghdasaryan, M. Al-Sheikh, and S. R. Sadda, “Choriocapillaris Imaging Using Multiple En Face Optical Coherence Tomography Angiography Image Averaging,” JAMA Ophthalmol. 135(11), 1197–1204 (2017).
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E. Borrelli, A. Uji, D. Sarraf, and S. R. Sadda, “Alterations in the choriocapillaris in intermediate age-related macular degeneration,” Invest. Ophthalmol. Vis. Sci. 58(11), 4792–4798 (2017).
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I. Stalmans, E. Vandewalle, D. R. Anderson, V. P. Costa, R. E. P. Frenkel, G. Garhofer, J. Grunwald, K. Gugleta, A. Harris, C. Hudson, I. Januleviciene, L. Kagemann, H. Kergoat, J. V. Lovasik, I. Lanzl, A. Martinez, Q. D. Nguyen, N. Plange, H. A. Reitsamer, M. Sehi, B. Siesky, O. Zeitz, S. Orgül, and L. Schmetterer, “Use of colour Doppler imaging in ocular blood flow research,” Acta Ophthalmol. 89(8), e609–e630 (2011).
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R. A. Linsenmeier and H. F. Zhang, “Retinal oxygen: from animals to humans,” Prog. Retin. Eye Res. 58, 115–151 (2017).
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Q. Zhang, F. Zheng, E. H. Motulsky, G. Gregori, Z. Chu, C. L. Chen, C. Li, L. de Sisternes, M. Durbin, P. J. Rosenfeld, and R. K. Wang, “A novel strategy for quantifying choriocapillaris flow voids using swept-source OCT angiography,” Invest. Ophthalmol. Vis. Sci. 59(1), 203–211 (2018).
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M. A. Zouache, I. Eames, C. A. Klettner, and P. J. Luthert, “Form, shape and function: segmented blood flow in the choriocapillaris,” Sci. Rep. 6(1), 35754 (2016).
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T. Sugiyama, M. Araie, C. E. Riva, L. Schmetterer, and S. Orgul, “Use of laser speckle flowgraphy in ocular blood flow research,” Acta Ophthalmol. 88(7), 723–729 (2010).
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P. L. Nesper, B. T. Soetikno, and A. A. Fawzi, “Choriocapillaris nonperfusion is associated with poor visual acuity in eyes with reticular pseudodrusen,” Am. J. Ophthalmol. 174, 42–55 (2017).
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R. F. Spaide, “Choriocapillaris flow features follow a power law distribution: implications for characterization and mechanisms of disease progression,” Am. J. Ophthalmol. 170, 58–67 (2016).
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P. L. Nesper, B. T. Soetikno, and A. A. Fawzi, “Choriocapillaris nonperfusion is associated with poor visual acuity in eyes with reticular pseudodrusen,” Am. J. Ophthalmol. 174, 42–55 (2017).
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A. Boltz, A. Luksch, B. Wimpissinger, N. Maar, G. Weigert, S. Frantal, W. Brannath, G. Garhöfer, E. Ergun, M. Stur, and L. Schmetterer, “Choroidal blood flow and progression of age-related macular degeneration in the fellow eye in patients with unilateral choroidal neovascularization,” Invest. Ophthalmol. Vis. Sci. 51(8), 4220–4225 (2010).
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M. Nicolò, R. Rosa, D. Musetti, M. Musolino, M. Saccheggiani, and C. E. Traverso, “Choroidal vascular flow area in central serous chorioretinopathy using swept-source optical coherence tomography angiography,” Invest. Ophthalmol. Vis. Sci. 58(4), 2002–2010 (2017).
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P. L. Nesper, P. K. Roberts, A. C. Onishi, H. Chai, L. Liu, L. M. Jampol, and A. A. Fawzi, “Quantifying microvascular abnormalities with increasing severity of diabetic retinopathy using optical coherence tomography angiography,” Invest. Ophthalmol. Vis. Sci. 58(6), BIO307 (2017).
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M. Hirata, A. Tsujikawa, A. Matsumoto, M. Hangai, S. Ooto, K. Yamashiro, M. Akiba, and N. Yoshimura, “Macular choroidal thickness and volume in normal subjects measured by swept-source optical coherence tomography,” Invest. Ophthalmol. Vis. Sci. 52(8), 4971–4978 (2011).
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E. Borrelli, A. Uji, D. Sarraf, and S. R. Sadda, “Alterations in the choriocapillaris in intermediate age-related macular degeneration,” Invest. Ophthalmol. Vis. Sci. 58(11), 4792–4798 (2017).
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L. An, T. T. Shen, and R. K. Wang, “Using ultrahigh sensitive optical microangiography to achieve comprehensive depth resolved microvasculature mapping for human retina,” J. Biomed. Opt. 16(10), 106013 (2011).
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R. A. Linsenmeier and H. F. Zhang, “Retinal oxygen: from animals to humans,” Prog. Retin. Eye Res. 58, 115–151 (2017).
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A. H. Kashani, C.-L. Chen, J. K. Gahm, F. Zheng, G. M. Richter, P. J. Rosenfeld, Y. Shi, and R. K. Wang, “Optical coherence tomography angiography: A comprehensive review of current methods and clinical applications,” Prog. Retin. Eye Res. 60, 66–100 (2017).
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R. A. Leitgeb, R. M. Werkmeister, C. Blatter, and L. Schmetterer, “Doppler optical coherence tomography,” Prog. Retin. Eye Res. 41, 26–43 (2014).
[Crossref] [PubMed]

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E. Borrelli, E. H. Souied, K. B. Freund, G. Querques, A. Miere, O. Gal-Or, R. Sacconi, S. R. Sadda, and D. Sarraf, “Reduced choriocapillaris flow in eyes with type 3 neovascularization and age- related macular degeneration,” Retina 38(10), 1968–1976 (2018).
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[Crossref] [PubMed]

Sci. Rep. (1)

M. A. Zouache, I. Eames, C. A. Klettner, and P. J. Luthert, “Form, shape and function: segmented blood flow in the choriocapillaris,” Sci. Rep. 6(1), 35754 (2016).
[Crossref] [PubMed]

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M. A. Kirby, C. Li, W. J. Choi, G. Gregori, P. Rosenfeld, and R. Wang, “Why choroid vessels appear dark in clinical OCT images,” in Ophthalmic Technologies XXVIII (2018), 10474, pp. 1047425–1047428.

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Figures (10)

Fig. 1
Fig. 1 The schematic of imaging sampling by point scan mode. An-1, An and An + 1 refer to three adjacent A-scans. ε is the lateral resolution of the system. ∆L is the lateral shift between adjacent A-scans. The sampling rate is defined as ε/∆L.
Fig. 2
Fig. 2 Angiographic and structural enface choriocapillaris images max projected from 10 µm slab and 3 µm slab.
Fig. 3
Fig. 3 a) an image of choriocapillaris taken from the retina side at the posterior pole of a human donor eye using a high resolution confocal microscopy. The image was modified from [21]. b) an uncompensated image of choriocapillaris taken at the fovea of a non-human primate eye. The image was cropped to the same size as a) from a 3 × 3 mm2 image. Yellow arrows indicate the appearance of deeper choroidal vessels using both methods. White arrow indicates a flow void. Scale bar: 200 µm.
Fig. 4
Fig. 4 Illustration of flow void segmentation method. (a-b) Angiographic and structural enface images of the choriocapillaris. (c) The variance of the adjusted image reaches its minimum when n equal to 0.2 in this particular image. (d) The adjusted choriocapillaris image where the dark region from the deep choroidal vessels is compensated. (e) The choriocapillaris with flow voids labeled in red while the threshold level is set to be I adj ¯ 1.5×SD( I adj ) from the grayscale histogram of the image (f). The intensity profiles of the yellow lines in uncompensated (a) and compensated (d) choriocapillaris images are plotted in (g). The low intensity region affected by the deep choroidal vessels is compensated (gray region in the plot), while the overall contrast is not changed.
Fig. 5
Fig. 5 Illustration of two different downsampling methods. (a) The concept demonstration to convert a 4 × 4 grid to a 2 × 2 grid. (b) A sample choriocapillaris image downsampled by a factor of 2 with both methods.
Fig. 6
Fig. 6 The demonstration of applying different flow void segmentation algorithms on a 3 × 3 mm2 choriocapillaris image centered at the fovea. (a) Borrelli et al. [34] used the global threshold method where the threshold level was set to be the mean intensity of the avascular outer retinal layer. (b) Nicolo et al. [24] applied Otsu’s thresholding method. (c) Spaide [26]. used Phansalkar local threshold method. (d-e) Zhang et al. [29] used the structural image to compensate the angiogram, and then used mean-1SD and mean-1.5SD to binaries the compensated images.
Fig. 7
Fig. 7 Repeated measurements from both eyes of a non-human primate. Inter-eye differences in choriocapillaris due to an unknown reason are noticed. The adjusted choriocapillaris images are shown in a-c) and g-i), and the images with choriocapillaris with flow voids segmented are shown in d-f) and j-l).
Fig. 8
Fig. 8 A 3 × 3 mm2 choriocapillaris image centered at the fovea downsampled by factors of 2, 6 and 10 using both neighborhood averaging (a-c) and spatial pooling (d-f) methods, which correspond to the pixel resolutions of 6 μm, 18 μm and 30 μm, respectively. Over an increase of the pixel resolution, the flow void density maintains at a relatively consistent level (g), and flow void sizes increase progressive using both methods.
Fig. 9
Fig. 9 (a) The original choriocapillaris image. (b) the choriocapillaris image overlaid with the segmented flow voids (red). (c) The flow void density distribution map generated from (b), while the flow voids were shown in black color for better visualization. (d) A 3 × 3 mm2 area cropped around the fovea from the wide field image, and the flow void density within is 8.28%, where for the same region, the corresponding flow void density from a densely sampled 3 × 3 mm2 protocol is 7.48%. (e) Statistical comparison of the same 3 × 3 mm2 area acquired from acquired by 3 × 3 mm2 protocol, 12 × 12 mm2 without uneven illuminance and 12 × 12 mm2 with uneven illuminance compensation. Data are shown as mean ± SD.
Fig. 10
Fig. 10 Wide field flow void distribution from eleven eyes (N = 11). (a) The averaged flow void density map. (b) Flow void density at different distances to the fovea. ONH was excluded manually in the density calculation.

Tables (3)

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Table 1 A summary of thicknesses of choriocapillaris segmentations from previous studies.

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Table 2 The Choriocapillaris Imaging Protocols

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Table 3 Statistical results of flow void density on a 3 × 3 mm2 area centered at the fovea using different segment methods. For calculating the flow void density from all studied eyes (N = 11) were analyzed. Intraclass correlation coefficients (ICC) were calculated from three repeated measurements in three animals.

Equations (2)

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I adjusted = I OCTA ( I Morph ) n .
n= min n' ( I adj I adj ¯ ) 2 N .

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