Abstract

The zebrafish is a robust model for studying human ophthalmic function and disease because of its fecundity, life-cycle, and similarities between its retinal structure and the human retina. Here, we demonstrate longitudinal in vivo imaging of retinal structure using optical coherence tomography (OCT) and noninvasive retinal vascular perfusion imaging using OCT angiography (OCT-A) in zebrafish. In addition, we present methods for retinal vascular segmentation and biometry to quantify vessel branch length, curvature, and angle. We further motivate retinal vascular biometry as a novel method for noninvasive zebrafish identification and demonstrated 99.9% accuracy for uniquely identifying eyes from a set of 200 longitudinal OCT/OCT-A volumes. The described methods enable the quantitative analysis of the vascular changes in zebrafish models of ophthalmic diseases and may broadly benefit large-scale zebrafish studies.

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

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2017 (1)

T. Wecker, C. Ehlken, A. Bühler, C. Lange, H. Agostini, D. Böhringer, and A. Stahl, “Five-year visual acuity outcomes and injection patterns in patients with pro-re-nata treatments for AMD, DME, RVO and myopic CNV,” Br. J. Ophthalmol. 101(3), 353–359 (2017).
[Crossref] [PubMed]

2016 (3)

B. Heimes, F. Gunnemann, M. Ziegler, M. Gutfleisch, G. Spital, D. Pauleikhoff, and A. Lommatzsch, “Compliance von Patienten mit altersabhängiger Makuladegeneration unter Anti-VEGF-Therapie:Analyse und Verbesserungsvorschläge,” Ophthalmologe 113(11), 925–932 (2016).
[Crossref] [PubMed]

M. M. Sachdeva, A. Moshiri, H. A. Leder, and A. W. Scott, “Endophthalmitis following intravitreal injection of anti-VEGF agents: long-term outcomes and the identification of unusual micro-organisms,” J. Ophthalmic Inflamm. Infect. 6(1), 2 (2016).
[Crossref] [PubMed]

B. A. Bell, A. Yuan, R. M. Dicicco, J. Fogerty, E. M. Lessieur, and B. D. Perkins, “The adult zebrafish retina: In vivo optical sectioning with Confocal Scanning Laser Ophthalmoscopy and Spectral-Domain Optical Coherence Tomography,” Exp. Eye Res. 153, 65–78 (2016).
[Crossref] [PubMed]

2015 (2)

2014 (3)

B. A. Bell, J. Xie, A. Yuan, C. Kaul, J. G. Hollyfield, and B. Anand-Apte, “Retinal Vasculature of Adult Zebrafish: In Vivo Imaging Using Confocal Scanning Laser Ophthalmoscopy,” Exp. Eye Res. 129, 107–118 (2014).
[Crossref] [PubMed]

R. M. DiCicco, B. A. Bell, C. Kaul, J. G. Hollyfield, B. Anand-Apte, B. D. Perkins, Y. K. Tao, and A. Yuan, “Retinal regeneration following OCT-guided laser injury in zebrafish,” Invest. Ophthalmol. Vis. Sci. 55(10), 6281–6288 (2014).
[Crossref] [PubMed]

J. Chhetri, G. Jacobson, and N. Gueven, “Zebrafishon the move towards ophthalmological research,” Eye (Lond.) 28(4), 367–380 (2014).
[Crossref] [PubMed]

2013 (2)

K. G. Falavarjani and Q. D. Nguyen, “Adverse events and complications associated with intravitreal injection of anti-VEGF agents: a review of literature,” Eye (Lond.) 27(7), 787–794 (2013).
[Crossref] [PubMed]

S. Rofagha, R. B. Bhisitkul, D. S. Boyer, S. R. Sadda, and K. Zhang, “Seven-Year Outcomes in Ranibizumab-Treated Patients in ANCHOR, MARINA, and HORIZON: A Multicenter Cohort Study (SEVEN-UP),” Ophthalmology 120(11), 2292–2299 (2013).
[Crossref] [PubMed]

2012 (2)

J. L. Kovach, S. G. Schwartz, H. W. Flynn, and I. U. Scott, “Anti-VEGF Treatment Strategies for Wet AMD,” J. Ophthalmol. 2012, 786870 (2012).
[Crossref] [PubMed]

T. Y. Chang, C. Pardo-Martin, A. Allalou, C. Wählby, and M. F. Yanik, “Fully automated cellular-resolution vertebrate screening platform with parallel animal processing,” Lab Chip 12(4), 711–716 (2012).
[Crossref] [PubMed]

2011 (4)

J. Bibliowicz, R. K. Tittle, and J. M. Gross, “Toward a better understanding of human eye disease insights from the zebrafish, Danio rerio,” Prog. Mol. Biol. Transl. Sci. 100, 287–330 (2011).
[Crossref] [PubMed]

R. Tadayoni, E. Vicaut, F. Devin, C. Creuzot-Garcher, J. P. Berrod, Y. Le Mer, J. F. Korobelnik, M. Aout, P. Massin, and A. Gaudric, “A randomized controlled trial of alleviated positioning after small macular hole surgery,” Ophthalmology 118(1), 150–155 (2011).
[Crossref] [PubMed]

D. F. Martin, M. G. Maguire, G. S. Ying, J. E. Grunwald, S. L. Fine, and G. J. Jaffe, “Ranibizumab and Bevacizumab for Neovascular Age-Related Macular Degeneration,” N. Engl. J. Med. 364(20), 1897–1908 (2011).
[Crossref] [PubMed]

A. L. Menke, J. M. Spitsbergen, A. P. M. Wolterbeek, and R. A. Woutersen, “Normal anatomy and histology of the adult zebrafish,” Toxicol. Pathol. 39(5), 759–775 (2011).
[Crossref] [PubMed]

2010 (2)

2009 (1)

D. B. Rein, J. S. Wittenborn, X. Zhang, A. A. Honeycutt, S. B. Lesesne, and J. Saaddine, “Forecasting age-related macular degeneration through the year 2050: The potential impact of new treatments,” Arch. Ophthalmol. 127(4), 533–540 (2009).
[Crossref] [PubMed]

2008 (4)

R. Simó and C. Hernández, “Intravitreous anti-VEGF for diabetic retinopathy: hopes and fears for a new therapeutic strategy,” Diabetologia 51(9), 1574–1580 (2008).
[Crossref] [PubMed]

J. M. Fadool and J. E. Dowling, “Zebrafish: A model system for the study of eye genetics,” Prog. Retin. Eye Res. 27(1), 89–110 (2008).
[Crossref] [PubMed]

L. An and R. K. Wang, “In vivo volumetric imaging of vascular perfusion within human retina and choroids with optical micro-angiography,” Opt. Express 16(15), 11438–11452 (2008).
[Crossref] [PubMed]

M. Guizar-Sicairos, S. T. Thurman, and J. R. Fienup, “Efficient subpixel image registration algorithms,” Opt. Lett. 33(2), 156–158 (2008).
[Crossref] [PubMed]

2007 (1)

Y. Alvarez, M. L. Cederlund, D. C. Cottell, B. R. Bill, S. C. Ekker, J. Torres-Vazquez, B. M. Weinstein, D. R. Hyde, T. S. Vihtelic, and B. N. Kennedy, “Genetic determinants of hyaloid and retinal vasculature in zebrafish,” BMC Dev. Biol. 7(1), 114 (2007).
[Crossref] [PubMed]

2006 (1)

K. D. Rao, Y. Verma, H. Patel, and P. Gupta, “Non-invasive ophthalmic imaging of adult zebrafish eye using optical coherence tomography,” CURRENT SCIENCE-BANGALORE 90, 1506 (2006).

2005 (1)

L. I. Zon and R. T. Peterson, “In vivo drug discovery in the zebrafish,” Nat. Rev. Drug Discov. 4(1), 35–44 (2005).
[Crossref] [PubMed]

2004 (4)

K. B. Shah and D. P. Han, “Proliferative diabetic retinopathy,” Int. Ophthalmol. Clin. 44(4), 69–84 (2004).
[Crossref] [PubMed]

E. S. Gragoudas, A. P. Adamis, E. T. Cunningham, M. Feinsod, and D. R. Guyer, “Pegaptanib for neovascular age-related macular degeneration,” N. Engl. J. Med. 351(27), 2805–2816 (2004).
[Crossref] [PubMed]

D. S. Friedman, B. J. O’Colmain, B. Muñoz, S. C. Tomany, C. McCarty, P. T. de Jong, B. Nemesure, P. Mitchell, and J. Kempen, “Prevalence of age-related macular degeneration in the United States,” Arch. Ophthalmol. 122(4), 564–572 (2004).
[Crossref] [PubMed]

P. Goldsmith, “Zebrafish as a pharmacological tool: the how, why and when,” Curr. Opin. Pharmacol. 4(5), 504–512 (2004).
[Crossref] [PubMed]

2003 (1)

A. L. Rubinstein, “Zebrafish: from disease modeling to drug discovery,” Curr. Opin. Drug Discov. Devel. 6(2), 218–223 (2003).
[PubMed]

2002 (1)

A. Ringholm, R. Fredriksson, N. Poliakova, Y.-L. Yan, J. H. Postlethwait, D. Larhammar, and H. B. Schiöth, “One melanocortin 4 and two melanocortin 5 receptors from zebrafish show remarkable conservation in structure and pharmacology,” J. Neurochem. 82(1), 6–18 (2002).
[Crossref] [PubMed]

2001 (1)

S. Isogai, M. Horiguchi, and B. M. Weinstein, “The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development,” Dev. Biol. 230(2), 278–301 (2001).
[Crossref] [PubMed]

1997 (1)

D. S. Weile and E. Michielssen, “Genetic algorithm optimization applied to electromagnetics: a review,” IEEE Trans. Antenn. Propag. 45(3), 343–353 (1997).
[Crossref]

1995 (1)

S. Chen and R. M. Haralick, “Recursive erosion, dilation, opening, and closing transforms,” IEEE Trans. Image Process. 4(3), 335–345 (1995).
[Crossref] [PubMed]

1991 (1)

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

Adamis, A. P.

E. S. Gragoudas, A. P. Adamis, E. T. Cunningham, M. Feinsod, and D. R. Guyer, “Pegaptanib for neovascular age-related macular degeneration,” N. Engl. J. Med. 351(27), 2805–2816 (2004).
[Crossref] [PubMed]

Agostini, H.

T. Wecker, C. Ehlken, A. Bühler, C. Lange, H. Agostini, D. Böhringer, and A. Stahl, “Five-year visual acuity outcomes and injection patterns in patients with pro-re-nata treatments for AMD, DME, RVO and myopic CNV,” Br. J. Ophthalmol. 101(3), 353–359 (2017).
[Crossref] [PubMed]

Allalou, A.

T. Y. Chang, C. Pardo-Martin, A. Allalou, C. Wählby, and M. F. Yanik, “Fully automated cellular-resolution vertebrate screening platform with parallel animal processing,” Lab Chip 12(4), 711–716 (2012).
[Crossref] [PubMed]

Alvarez, Y.

Y. Alvarez, M. L. Cederlund, D. C. Cottell, B. R. Bill, S. C. Ekker, J. Torres-Vazquez, B. M. Weinstein, D. R. Hyde, T. S. Vihtelic, and B. N. Kennedy, “Genetic determinants of hyaloid and retinal vasculature in zebrafish,” BMC Dev. Biol. 7(1), 114 (2007).
[Crossref] [PubMed]

An, L.

Anand-Apte, B.

B. A. Bell, J. Xie, A. Yuan, C. Kaul, J. G. Hollyfield, and B. Anand-Apte, “Retinal Vasculature of Adult Zebrafish: In Vivo Imaging Using Confocal Scanning Laser Ophthalmoscopy,” Exp. Eye Res. 129, 107–118 (2014).
[Crossref] [PubMed]

R. M. DiCicco, B. A. Bell, C. Kaul, J. G. Hollyfield, B. Anand-Apte, B. D. Perkins, Y. K. Tao, and A. Yuan, “Retinal regeneration following OCT-guided laser injury in zebrafish,” Invest. Ophthalmol. Vis. Sci. 55(10), 6281–6288 (2014).
[Crossref] [PubMed]

Aout, M.

R. Tadayoni, E. Vicaut, F. Devin, C. Creuzot-Garcher, J. P. Berrod, Y. Le Mer, J. F. Korobelnik, M. Aout, P. Massin, and A. Gaudric, “A randomized controlled trial of alleviated positioning after small macular hole surgery,” Ophthalmology 118(1), 150–155 (2011).
[Crossref] [PubMed]

Araie, M.

Bell, B. A.

B. A. Bell, A. Yuan, R. M. Dicicco, J. Fogerty, E. M. Lessieur, and B. D. Perkins, “The adult zebrafish retina: In vivo optical sectioning with Confocal Scanning Laser Ophthalmoscopy and Spectral-Domain Optical Coherence Tomography,” Exp. Eye Res. 153, 65–78 (2016).
[Crossref] [PubMed]

R. M. DiCicco, B. A. Bell, C. Kaul, J. G. Hollyfield, B. Anand-Apte, B. D. Perkins, Y. K. Tao, and A. Yuan, “Retinal regeneration following OCT-guided laser injury in zebrafish,” Invest. Ophthalmol. Vis. Sci. 55(10), 6281–6288 (2014).
[Crossref] [PubMed]

B. A. Bell, J. Xie, A. Yuan, C. Kaul, J. G. Hollyfield, and B. Anand-Apte, “Retinal Vasculature of Adult Zebrafish: In Vivo Imaging Using Confocal Scanning Laser Ophthalmoscopy,” Exp. Eye Res. 129, 107–118 (2014).
[Crossref] [PubMed]

Berrod, J. P.

R. Tadayoni, E. Vicaut, F. Devin, C. Creuzot-Garcher, J. P. Berrod, Y. Le Mer, J. F. Korobelnik, M. Aout, P. Massin, and A. Gaudric, “A randomized controlled trial of alleviated positioning after small macular hole surgery,” Ophthalmology 118(1), 150–155 (2011).
[Crossref] [PubMed]

Bhisitkul, R. B.

S. Rofagha, R. B. Bhisitkul, D. S. Boyer, S. R. Sadda, and K. Zhang, “Seven-Year Outcomes in Ranibizumab-Treated Patients in ANCHOR, MARINA, and HORIZON: A Multicenter Cohort Study (SEVEN-UP),” Ophthalmology 120(11), 2292–2299 (2013).
[Crossref] [PubMed]

Bibliowicz, J.

J. Bibliowicz, R. K. Tittle, and J. M. Gross, “Toward a better understanding of human eye disease insights from the zebrafish, Danio rerio,” Prog. Mol. Biol. Transl. Sci. 100, 287–330 (2011).
[Crossref] [PubMed]

Bill, B. R.

Y. Alvarez, M. L. Cederlund, D. C. Cottell, B. R. Bill, S. C. Ekker, J. Torres-Vazquez, B. M. Weinstein, D. R. Hyde, T. S. Vihtelic, and B. N. Kennedy, “Genetic determinants of hyaloid and retinal vasculature in zebrafish,” BMC Dev. Biol. 7(1), 114 (2007).
[Crossref] [PubMed]

Böhringer, D.

T. Wecker, C. Ehlken, A. Bühler, C. Lange, H. Agostini, D. Böhringer, and A. Stahl, “Five-year visual acuity outcomes and injection patterns in patients with pro-re-nata treatments for AMD, DME, RVO and myopic CNV,” Br. J. Ophthalmol. 101(3), 353–359 (2017).
[Crossref] [PubMed]

Boyer, D. S.

S. Rofagha, R. B. Bhisitkul, D. S. Boyer, S. R. Sadda, and K. Zhang, “Seven-Year Outcomes in Ranibizumab-Treated Patients in ANCHOR, MARINA, and HORIZON: A Multicenter Cohort Study (SEVEN-UP),” Ophthalmology 120(11), 2292–2299 (2013).
[Crossref] [PubMed]

Bühler, A.

T. Wecker, C. Ehlken, A. Bühler, C. Lange, H. Agostini, D. Böhringer, and A. Stahl, “Five-year visual acuity outcomes and injection patterns in patients with pro-re-nata treatments for AMD, DME, RVO and myopic CNV,” Br. J. Ophthalmol. 101(3), 353–359 (2017).
[Crossref] [PubMed]

Cao, Y.

Z. Cao, L. D. Jensen, P. Rouhi, K. Hosaka, T. Länne, J. F. Steffensen, E. Wahlberg, and Y. Cao, “Hypoxia-induced retinopathy model in adult zebrafish,” Nat. Protoc. 5(12), 1903–1910 (2010).
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Cao, Z.

Z. Cao, L. D. Jensen, P. Rouhi, K. Hosaka, T. Länne, J. F. Steffensen, E. Wahlberg, and Y. Cao, “Hypoxia-induced retinopathy model in adult zebrafish,” Nat. Protoc. 5(12), 1903–1910 (2010).
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Cederlund, M. L.

Y. Alvarez, M. L. Cederlund, D. C. Cottell, B. R. Bill, S. C. Ekker, J. Torres-Vazquez, B. M. Weinstein, D. R. Hyde, T. S. Vihtelic, and B. N. Kennedy, “Genetic determinants of hyaloid and retinal vasculature in zebrafish,” BMC Dev. Biol. 7(1), 114 (2007).
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Chang, T. Y.

T. Y. Chang, C. Pardo-Martin, A. Allalou, C. Wählby, and M. F. Yanik, “Fully automated cellular-resolution vertebrate screening platform with parallel animal processing,” Lab Chip 12(4), 711–716 (2012).
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D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
[Crossref] [PubMed]

Chen, S.

S. Chen and R. M. Haralick, “Recursive erosion, dilation, opening, and closing transforms,” IEEE Trans. Image Process. 4(3), 335–345 (1995).
[Crossref] [PubMed]

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J. Chhetri, G. Jacobson, and N. Gueven, “Zebrafishon the move towards ophthalmological research,” Eye (Lond.) 28(4), 367–380 (2014).
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Cottell, D. C.

Y. Alvarez, M. L. Cederlund, D. C. Cottell, B. R. Bill, S. C. Ekker, J. Torres-Vazquez, B. M. Weinstein, D. R. Hyde, T. S. Vihtelic, and B. N. Kennedy, “Genetic determinants of hyaloid and retinal vasculature in zebrafish,” BMC Dev. Biol. 7(1), 114 (2007).
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Creuzot-Garcher, C.

R. Tadayoni, E. Vicaut, F. Devin, C. Creuzot-Garcher, J. P. Berrod, Y. Le Mer, J. F. Korobelnik, M. Aout, P. Massin, and A. Gaudric, “A randomized controlled trial of alleviated positioning after small macular hole surgery,” Ophthalmology 118(1), 150–155 (2011).
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Cunningham, E. T.

E. S. Gragoudas, A. P. Adamis, E. T. Cunningham, M. Feinsod, and D. R. Guyer, “Pegaptanib for neovascular age-related macular degeneration,” N. Engl. J. Med. 351(27), 2805–2816 (2004).
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D. S. Friedman, B. J. O’Colmain, B. Muñoz, S. C. Tomany, C. McCarty, P. T. de Jong, B. Nemesure, P. Mitchell, and J. Kempen, “Prevalence of age-related macular degeneration in the United States,” Arch. Ophthalmol. 122(4), 564–572 (2004).
[Crossref] [PubMed]

Devin, F.

R. Tadayoni, E. Vicaut, F. Devin, C. Creuzot-Garcher, J. P. Berrod, Y. Le Mer, J. F. Korobelnik, M. Aout, P. Massin, and A. Gaudric, “A randomized controlled trial of alleviated positioning after small macular hole surgery,” Ophthalmology 118(1), 150–155 (2011).
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Dicicco, R. M.

B. A. Bell, A. Yuan, R. M. Dicicco, J. Fogerty, E. M. Lessieur, and B. D. Perkins, “The adult zebrafish retina: In vivo optical sectioning with Confocal Scanning Laser Ophthalmoscopy and Spectral-Domain Optical Coherence Tomography,” Exp. Eye Res. 153, 65–78 (2016).
[Crossref] [PubMed]

R. M. DiCicco, B. A. Bell, C. Kaul, J. G. Hollyfield, B. Anand-Apte, B. D. Perkins, Y. K. Tao, and A. Yuan, “Retinal regeneration following OCT-guided laser injury in zebrafish,” Invest. Ophthalmol. Vis. Sci. 55(10), 6281–6288 (2014).
[Crossref] [PubMed]

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J. M. Fadool and J. E. Dowling, “Zebrafish: A model system for the study of eye genetics,” Prog. Retin. Eye Res. 27(1), 89–110 (2008).
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T. Wecker, C. Ehlken, A. Bühler, C. Lange, H. Agostini, D. Böhringer, and A. Stahl, “Five-year visual acuity outcomes and injection patterns in patients with pro-re-nata treatments for AMD, DME, RVO and myopic CNV,” Br. J. Ophthalmol. 101(3), 353–359 (2017).
[Crossref] [PubMed]

Ekker, S. C.

Y. Alvarez, M. L. Cederlund, D. C. Cottell, B. R. Bill, S. C. Ekker, J. Torres-Vazquez, B. M. Weinstein, D. R. Hyde, T. S. Vihtelic, and B. N. Kennedy, “Genetic determinants of hyaloid and retinal vasculature in zebrafish,” BMC Dev. Biol. 7(1), 114 (2007).
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J. M. Fadool and J. E. Dowling, “Zebrafish: A model system for the study of eye genetics,” Prog. Retin. Eye Res. 27(1), 89–110 (2008).
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K. G. Falavarjani and Q. D. Nguyen, “Adverse events and complications associated with intravitreal injection of anti-VEGF agents: a review of literature,” Eye (Lond.) 27(7), 787–794 (2013).
[Crossref] [PubMed]

Feinsod, M.

E. S. Gragoudas, A. P. Adamis, E. T. Cunningham, M. Feinsod, and D. R. Guyer, “Pegaptanib for neovascular age-related macular degeneration,” N. Engl. J. Med. 351(27), 2805–2816 (2004).
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Fienup, J. R.

Fine, S. L.

D. F. Martin, M. G. Maguire, G. S. Ying, J. E. Grunwald, S. L. Fine, and G. J. Jaffe, “Ranibizumab and Bevacizumab for Neovascular Age-Related Macular Degeneration,” N. Engl. J. Med. 364(20), 1897–1908 (2011).
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D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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J. L. Kovach, S. G. Schwartz, H. W. Flynn, and I. U. Scott, “Anti-VEGF Treatment Strategies for Wet AMD,” J. Ophthalmol. 2012, 786870 (2012).
[Crossref] [PubMed]

Fogerty, J.

B. A. Bell, A. Yuan, R. M. Dicicco, J. Fogerty, E. M. Lessieur, and B. D. Perkins, “The adult zebrafish retina: In vivo optical sectioning with Confocal Scanning Laser Ophthalmoscopy and Spectral-Domain Optical Coherence Tomography,” Exp. Eye Res. 153, 65–78 (2016).
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A. Ringholm, R. Fredriksson, N. Poliakova, Y.-L. Yan, J. H. Postlethwait, D. Larhammar, and H. B. Schiöth, “One melanocortin 4 and two melanocortin 5 receptors from zebrafish show remarkable conservation in structure and pharmacology,” J. Neurochem. 82(1), 6–18 (2002).
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D. S. Friedman, B. J. O’Colmain, B. Muñoz, S. C. Tomany, C. McCarty, P. T. de Jong, B. Nemesure, P. Mitchell, and J. Kempen, “Prevalence of age-related macular degeneration in the United States,” Arch. Ophthalmol. 122(4), 564–572 (2004).
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Fujimoto, J. G.

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

R. Tadayoni, E. Vicaut, F. Devin, C. Creuzot-Garcher, J. P. Berrod, Y. Le Mer, J. F. Korobelnik, M. Aout, P. Massin, and A. Gaudric, “A randomized controlled trial of alleviated positioning after small macular hole surgery,” Ophthalmology 118(1), 150–155 (2011).
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P. Goldsmith, “Zebrafish as a pharmacological tool: the how, why and when,” Curr. Opin. Pharmacol. 4(5), 504–512 (2004).
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E. S. Gragoudas, A. P. Adamis, E. T. Cunningham, M. Feinsod, and D. R. Guyer, “Pegaptanib for neovascular age-related macular degeneration,” N. Engl. J. Med. 351(27), 2805–2816 (2004).
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D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science 254(5035), 1178–1181 (1991).
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J. Bibliowicz, R. K. Tittle, and J. M. Gross, “Toward a better understanding of human eye disease insights from the zebrafish, Danio rerio,” Prog. Mol. Biol. Transl. Sci. 100, 287–330 (2011).
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D. F. Martin, M. G. Maguire, G. S. Ying, J. E. Grunwald, S. L. Fine, and G. J. Jaffe, “Ranibizumab and Bevacizumab for Neovascular Age-Related Macular Degeneration,” N. Engl. J. Med. 364(20), 1897–1908 (2011).
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J. Chhetri, G. Jacobson, and N. Gueven, “Zebrafishon the move towards ophthalmological research,” Eye (Lond.) 28(4), 367–380 (2014).
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Gunnemann, F.

B. Heimes, F. Gunnemann, M. Ziegler, M. Gutfleisch, G. Spital, D. Pauleikhoff, and A. Lommatzsch, “Compliance von Patienten mit altersabhängiger Makuladegeneration unter Anti-VEGF-Therapie:Analyse und Verbesserungsvorschläge,” Ophthalmologe 113(11), 925–932 (2016).
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K. D. Rao, Y. Verma, H. Patel, and P. Gupta, “Non-invasive ophthalmic imaging of adult zebrafish eye using optical coherence tomography,” CURRENT SCIENCE-BANGALORE 90, 1506 (2006).

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B. Heimes, F. Gunnemann, M. Ziegler, M. Gutfleisch, G. Spital, D. Pauleikhoff, and A. Lommatzsch, “Compliance von Patienten mit altersabhängiger Makuladegeneration unter Anti-VEGF-Therapie:Analyse und Verbesserungsvorschläge,” Ophthalmologe 113(11), 925–932 (2016).
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Guyer, D. R.

E. S. Gragoudas, A. P. Adamis, E. T. Cunningham, M. Feinsod, and D. R. Guyer, “Pegaptanib for neovascular age-related macular degeneration,” N. Engl. J. Med. 351(27), 2805–2816 (2004).
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K. B. Shah and D. P. Han, “Proliferative diabetic retinopathy,” Int. Ophthalmol. Clin. 44(4), 69–84 (2004).
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Hangai, M.

Haralick, R. M.

S. Chen and R. M. Haralick, “Recursive erosion, dilation, opening, and closing transforms,” IEEE Trans. Image Process. 4(3), 335–345 (1995).
[Crossref] [PubMed]

Hee, M. R.

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

B. Heimes, F. Gunnemann, M. Ziegler, M. Gutfleisch, G. Spital, D. Pauleikhoff, and A. Lommatzsch, “Compliance von Patienten mit altersabhängiger Makuladegeneration unter Anti-VEGF-Therapie:Analyse und Verbesserungsvorschläge,” Ophthalmologe 113(11), 925–932 (2016).
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R. Simó and C. Hernández, “Intravitreous anti-VEGF for diabetic retinopathy: hopes and fears for a new therapeutic strategy,” Diabetologia 51(9), 1574–1580 (2008).
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Hollyfield, J. G.

B. A. Bell, J. Xie, A. Yuan, C. Kaul, J. G. Hollyfield, and B. Anand-Apte, “Retinal Vasculature of Adult Zebrafish: In Vivo Imaging Using Confocal Scanning Laser Ophthalmoscopy,” Exp. Eye Res. 129, 107–118 (2014).
[Crossref] [PubMed]

R. M. DiCicco, B. A. Bell, C. Kaul, J. G. Hollyfield, B. Anand-Apte, B. D. Perkins, Y. K. Tao, and A. Yuan, “Retinal regeneration following OCT-guided laser injury in zebrafish,” Invest. Ophthalmol. Vis. Sci. 55(10), 6281–6288 (2014).
[Crossref] [PubMed]

Honeycutt, A. A.

D. B. Rein, J. S. Wittenborn, X. Zhang, A. A. Honeycutt, S. B. Lesesne, and J. Saaddine, “Forecasting age-related macular degeneration through the year 2050: The potential impact of new treatments,” Arch. Ophthalmol. 127(4), 533–540 (2009).
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Hood, D. C.

Horiguchi, M.

S. Isogai, M. Horiguchi, and B. M. Weinstein, “The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development,” Dev. Biol. 230(2), 278–301 (2001).
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Hosaka, K.

Z. Cao, L. D. Jensen, P. Rouhi, K. Hosaka, T. Länne, J. F. Steffensen, E. Wahlberg, and Y. Cao, “Hypoxia-induced retinopathy model in adult zebrafish,” Nat. Protoc. 5(12), 1903–1910 (2010).
[Crossref] [PubMed]

Huang, D.

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

Huang, Y.

Hyde, D. R.

Y. Alvarez, M. L. Cederlund, D. C. Cottell, B. R. Bill, S. C. Ekker, J. Torres-Vazquez, B. M. Weinstein, D. R. Hyde, T. S. Vihtelic, and B. N. Kennedy, “Genetic determinants of hyaloid and retinal vasculature in zebrafish,” BMC Dev. Biol. 7(1), 114 (2007).
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Isogai, S.

S. Isogai, M. Horiguchi, and B. M. Weinstein, “The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development,” Dev. Biol. 230(2), 278–301 (2001).
[Crossref] [PubMed]

Jacobson, G.

J. Chhetri, G. Jacobson, and N. Gueven, “Zebrafishon the move towards ophthalmological research,” Eye (Lond.) 28(4), 367–380 (2014).
[Crossref] [PubMed]

Jaffe, G. J.

D. F. Martin, M. G. Maguire, G. S. Ying, J. E. Grunwald, S. L. Fine, and G. J. Jaffe, “Ranibizumab and Bevacizumab for Neovascular Age-Related Macular Degeneration,” N. Engl. J. Med. 364(20), 1897–1908 (2011).
[Crossref] [PubMed]

Jensen, L. D.

Z. Cao, L. D. Jensen, P. Rouhi, K. Hosaka, T. Länne, J. F. Steffensen, E. Wahlberg, and Y. Cao, “Hypoxia-induced retinopathy model in adult zebrafish,” Nat. Protoc. 5(12), 1903–1910 (2010).
[Crossref] [PubMed]

Kaul, C.

B. A. Bell, J. Xie, A. Yuan, C. Kaul, J. G. Hollyfield, and B. Anand-Apte, “Retinal Vasculature of Adult Zebrafish: In Vivo Imaging Using Confocal Scanning Laser Ophthalmoscopy,” Exp. Eye Res. 129, 107–118 (2014).
[Crossref] [PubMed]

R. M. DiCicco, B. A. Bell, C. Kaul, J. G. Hollyfield, B. Anand-Apte, B. D. Perkins, Y. K. Tao, and A. Yuan, “Retinal regeneration following OCT-guided laser injury in zebrafish,” Invest. Ophthalmol. Vis. Sci. 55(10), 6281–6288 (2014).
[Crossref] [PubMed]

Kempen, J.

D. S. Friedman, B. J. O’Colmain, B. Muñoz, S. C. Tomany, C. McCarty, P. T. de Jong, B. Nemesure, P. Mitchell, and J. Kempen, “Prevalence of age-related macular degeneration in the United States,” Arch. Ophthalmol. 122(4), 564–572 (2004).
[Crossref] [PubMed]

Kennedy, B. N.

Y. Alvarez, M. L. Cederlund, D. C. Cottell, B. R. Bill, S. C. Ekker, J. Torres-Vazquez, B. M. Weinstein, D. R. Hyde, T. S. Vihtelic, and B. N. Kennedy, “Genetic determinants of hyaloid and retinal vasculature in zebrafish,” BMC Dev. Biol. 7(1), 114 (2007).
[Crossref] [PubMed]

Korobelnik, J. F.

R. Tadayoni, E. Vicaut, F. Devin, C. Creuzot-Garcher, J. P. Berrod, Y. Le Mer, J. F. Korobelnik, M. Aout, P. Massin, and A. Gaudric, “A randomized controlled trial of alleviated positioning after small macular hole surgery,” Ophthalmology 118(1), 150–155 (2011).
[Crossref] [PubMed]

Kovach, J. L.

J. L. Kovach, S. G. Schwartz, H. W. Flynn, and I. U. Scott, “Anti-VEGF Treatment Strategies for Wet AMD,” J. Ophthalmol. 2012, 786870 (2012).
[Crossref] [PubMed]

Lange, C.

T. Wecker, C. Ehlken, A. Bühler, C. Lange, H. Agostini, D. Böhringer, and A. Stahl, “Five-year visual acuity outcomes and injection patterns in patients with pro-re-nata treatments for AMD, DME, RVO and myopic CNV,” Br. J. Ophthalmol. 101(3), 353–359 (2017).
[Crossref] [PubMed]

Länne, T.

Z. Cao, L. D. Jensen, P. Rouhi, K. Hosaka, T. Länne, J. F. Steffensen, E. Wahlberg, and Y. Cao, “Hypoxia-induced retinopathy model in adult zebrafish,” Nat. Protoc. 5(12), 1903–1910 (2010).
[Crossref] [PubMed]

Larhammar, D.

A. Ringholm, R. Fredriksson, N. Poliakova, Y.-L. Yan, J. H. Postlethwait, D. Larhammar, and H. B. Schiöth, “One melanocortin 4 and two melanocortin 5 receptors from zebrafish show remarkable conservation in structure and pharmacology,” J. Neurochem. 82(1), 6–18 (2002).
[Crossref] [PubMed]

Le Mer, Y.

R. Tadayoni, E. Vicaut, F. Devin, C. Creuzot-Garcher, J. P. Berrod, Y. Le Mer, J. F. Korobelnik, M. Aout, P. Massin, and A. Gaudric, “A randomized controlled trial of alleviated positioning after small macular hole surgery,” Ophthalmology 118(1), 150–155 (2011).
[Crossref] [PubMed]

Leder, H. A.

M. M. Sachdeva, A. Moshiri, H. A. Leder, and A. W. Scott, “Endophthalmitis following intravitreal injection of anti-VEGF agents: long-term outcomes and the identification of unusual micro-organisms,” J. Ophthalmic Inflamm. Infect. 6(1), 2 (2016).
[Crossref] [PubMed]

Lesesne, S. B.

D. B. Rein, J. S. Wittenborn, X. Zhang, A. A. Honeycutt, S. B. Lesesne, and J. Saaddine, “Forecasting age-related macular degeneration through the year 2050: The potential impact of new treatments,” Arch. Ophthalmol. 127(4), 533–540 (2009).
[Crossref] [PubMed]

Lessieur, E. M.

B. A. Bell, A. Yuan, R. M. Dicicco, J. Fogerty, E. M. Lessieur, and B. D. Perkins, “The adult zebrafish retina: In vivo optical sectioning with Confocal Scanning Laser Ophthalmoscopy and Spectral-Domain Optical Coherence Tomography,” Exp. Eye Res. 153, 65–78 (2016).
[Crossref] [PubMed]

Lin, C. P.

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

Lommatzsch, A.

B. Heimes, F. Gunnemann, M. Ziegler, M. Gutfleisch, G. Spital, D. Pauleikhoff, and A. Lommatzsch, “Compliance von Patienten mit altersabhängiger Makuladegeneration unter Anti-VEGF-Therapie:Analyse und Verbesserungsvorschläge,” Ophthalmologe 113(11), 925–932 (2016).
[Crossref] [PubMed]

MacRae, C. A.

C. A. MacRae and R. T. Peterson, “Zebrafish as tools for drug discovery,” Nat. Rev. Drug Discov. 14(10), 721–731 (2015).
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Maguire, M. G.

D. F. Martin, M. G. Maguire, G. S. Ying, J. E. Grunwald, S. L. Fine, and G. J. Jaffe, “Ranibizumab and Bevacizumab for Neovascular Age-Related Macular Degeneration,” N. Engl. J. Med. 364(20), 1897–1908 (2011).
[Crossref] [PubMed]

Martin, D. F.

D. F. Martin, M. G. Maguire, G. S. Ying, J. E. Grunwald, S. L. Fine, and G. J. Jaffe, “Ranibizumab and Bevacizumab for Neovascular Age-Related Macular Degeneration,” N. Engl. J. Med. 364(20), 1897–1908 (2011).
[Crossref] [PubMed]

Massin, P.

R. Tadayoni, E. Vicaut, F. Devin, C. Creuzot-Garcher, J. P. Berrod, Y. Le Mer, J. F. Korobelnik, M. Aout, P. Massin, and A. Gaudric, “A randomized controlled trial of alleviated positioning after small macular hole surgery,” Ophthalmology 118(1), 150–155 (2011).
[Crossref] [PubMed]

McCarty, C.

D. S. Friedman, B. J. O’Colmain, B. Muñoz, S. C. Tomany, C. McCarty, P. T. de Jong, B. Nemesure, P. Mitchell, and J. Kempen, “Prevalence of age-related macular degeneration in the United States,” Arch. Ophthalmol. 122(4), 564–572 (2004).
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A. L. Menke, J. M. Spitsbergen, A. P. M. Wolterbeek, and R. A. Woutersen, “Normal anatomy and histology of the adult zebrafish,” Toxicol. Pathol. 39(5), 759–775 (2011).
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D. S. Weile and E. Michielssen, “Genetic algorithm optimization applied to electromagnetics: a review,” IEEE Trans. Antenn. Propag. 45(3), 343–353 (1997).
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Mitchell, P.

D. S. Friedman, B. J. O’Colmain, B. Muñoz, S. C. Tomany, C. McCarty, P. T. de Jong, B. Nemesure, P. Mitchell, and J. Kempen, “Prevalence of age-related macular degeneration in the United States,” Arch. Ophthalmol. 122(4), 564–572 (2004).
[Crossref] [PubMed]

Moshiri, A.

M. M. Sachdeva, A. Moshiri, H. A. Leder, and A. W. Scott, “Endophthalmitis following intravitreal injection of anti-VEGF agents: long-term outcomes and the identification of unusual micro-organisms,” J. Ophthalmic Inflamm. Infect. 6(1), 2 (2016).
[Crossref] [PubMed]

Muñoz, B.

D. S. Friedman, B. J. O’Colmain, B. Muñoz, S. C. Tomany, C. McCarty, P. T. de Jong, B. Nemesure, P. Mitchell, and J. Kempen, “Prevalence of age-related macular degeneration in the United States,” Arch. Ophthalmol. 122(4), 564–572 (2004).
[Crossref] [PubMed]

Nemesure, B.

D. S. Friedman, B. J. O’Colmain, B. Muñoz, S. C. Tomany, C. McCarty, P. T. de Jong, B. Nemesure, P. Mitchell, and J. Kempen, “Prevalence of age-related macular degeneration in the United States,” Arch. Ophthalmol. 122(4), 564–572 (2004).
[Crossref] [PubMed]

Nguyen, Q. D.

K. G. Falavarjani and Q. D. Nguyen, “Adverse events and complications associated with intravitreal injection of anti-VEGF agents: a review of literature,” Eye (Lond.) 27(7), 787–794 (2013).
[Crossref] [PubMed]

O’Colmain, B. J.

D. S. Friedman, B. J. O’Colmain, B. Muñoz, S. C. Tomany, C. McCarty, P. T. de Jong, B. Nemesure, P. Mitchell, and J. Kempen, “Prevalence of age-related macular degeneration in the United States,” Arch. Ophthalmol. 122(4), 564–572 (2004).
[Crossref] [PubMed]

Pardo-Martin, C.

T. Y. Chang, C. Pardo-Martin, A. Allalou, C. Wählby, and M. F. Yanik, “Fully automated cellular-resolution vertebrate screening platform with parallel animal processing,” Lab Chip 12(4), 711–716 (2012).
[Crossref] [PubMed]

Patel, H.

K. D. Rao, Y. Verma, H. Patel, and P. Gupta, “Non-invasive ophthalmic imaging of adult zebrafish eye using optical coherence tomography,” CURRENT SCIENCE-BANGALORE 90, 1506 (2006).

Pauleikhoff, D.

B. Heimes, F. Gunnemann, M. Ziegler, M. Gutfleisch, G. Spital, D. Pauleikhoff, and A. Lommatzsch, “Compliance von Patienten mit altersabhängiger Makuladegeneration unter Anti-VEGF-Therapie:Analyse und Verbesserungsvorschläge,” Ophthalmologe 113(11), 925–932 (2016).
[Crossref] [PubMed]

Perkins, B. D.

B. A. Bell, A. Yuan, R. M. Dicicco, J. Fogerty, E. M. Lessieur, and B. D. Perkins, “The adult zebrafish retina: In vivo optical sectioning with Confocal Scanning Laser Ophthalmoscopy and Spectral-Domain Optical Coherence Tomography,” Exp. Eye Res. 153, 65–78 (2016).
[Crossref] [PubMed]

R. M. DiCicco, B. A. Bell, C. Kaul, J. G. Hollyfield, B. Anand-Apte, B. D. Perkins, Y. K. Tao, and A. Yuan, “Retinal regeneration following OCT-guided laser injury in zebrafish,” Invest. Ophthalmol. Vis. Sci. 55(10), 6281–6288 (2014).
[Crossref] [PubMed]

Peterson, R. T.

C. A. MacRae and R. T. Peterson, “Zebrafish as tools for drug discovery,” Nat. Rev. Drug Discov. 14(10), 721–731 (2015).
[Crossref] [PubMed]

L. I. Zon and R. T. Peterson, “In vivo drug discovery in the zebrafish,” Nat. Rev. Drug Discov. 4(1), 35–44 (2005).
[Crossref] [PubMed]

Poliakova, N.

A. Ringholm, R. Fredriksson, N. Poliakova, Y.-L. Yan, J. H. Postlethwait, D. Larhammar, and H. B. Schiöth, “One melanocortin 4 and two melanocortin 5 receptors from zebrafish show remarkable conservation in structure and pharmacology,” J. Neurochem. 82(1), 6–18 (2002).
[Crossref] [PubMed]

Postlethwait, J. H.

A. Ringholm, R. Fredriksson, N. Poliakova, Y.-L. Yan, J. H. Postlethwait, D. Larhammar, and H. B. Schiöth, “One melanocortin 4 and two melanocortin 5 receptors from zebrafish show remarkable conservation in structure and pharmacology,” J. Neurochem. 82(1), 6–18 (2002).
[Crossref] [PubMed]

Puliafito, C. A.

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

Rao, K. D.

K. D. Rao, Y. Verma, H. Patel, and P. Gupta, “Non-invasive ophthalmic imaging of adult zebrafish eye using optical coherence tomography,” CURRENT SCIENCE-BANGALORE 90, 1506 (2006).

Raza, A. S.

Rein, D. B.

D. B. Rein, J. S. Wittenborn, X. Zhang, A. A. Honeycutt, S. B. Lesesne, and J. Saaddine, “Forecasting age-related macular degeneration through the year 2050: The potential impact of new treatments,” Arch. Ophthalmol. 127(4), 533–540 (2009).
[Crossref] [PubMed]

Reisman, C. A.

Ringholm, A.

A. Ringholm, R. Fredriksson, N. Poliakova, Y.-L. Yan, J. H. Postlethwait, D. Larhammar, and H. B. Schiöth, “One melanocortin 4 and two melanocortin 5 receptors from zebrafish show remarkable conservation in structure and pharmacology,” J. Neurochem. 82(1), 6–18 (2002).
[Crossref] [PubMed]

Rofagha, S.

S. Rofagha, R. B. Bhisitkul, D. S. Boyer, S. R. Sadda, and K. Zhang, “Seven-Year Outcomes in Ranibizumab-Treated Patients in ANCHOR, MARINA, and HORIZON: A Multicenter Cohort Study (SEVEN-UP),” Ophthalmology 120(11), 2292–2299 (2013).
[Crossref] [PubMed]

Rouhi, P.

Z. Cao, L. D. Jensen, P. Rouhi, K. Hosaka, T. Länne, J. F. Steffensen, E. Wahlberg, and Y. Cao, “Hypoxia-induced retinopathy model in adult zebrafish,” Nat. Protoc. 5(12), 1903–1910 (2010).
[Crossref] [PubMed]

Rubinstein, A. L.

A. L. Rubinstein, “Zebrafish: from disease modeling to drug discovery,” Curr. Opin. Drug Discov. Devel. 6(2), 218–223 (2003).
[PubMed]

Saaddine, J.

D. B. Rein, J. S. Wittenborn, X. Zhang, A. A. Honeycutt, S. B. Lesesne, and J. Saaddine, “Forecasting age-related macular degeneration through the year 2050: The potential impact of new treatments,” Arch. Ophthalmol. 127(4), 533–540 (2009).
[Crossref] [PubMed]

Sachdeva, M. M.

M. M. Sachdeva, A. Moshiri, H. A. Leder, and A. W. Scott, “Endophthalmitis following intravitreal injection of anti-VEGF agents: long-term outcomes and the identification of unusual micro-organisms,” J. Ophthalmic Inflamm. Infect. 6(1), 2 (2016).
[Crossref] [PubMed]

Sadda, S. R.

S. Rofagha, R. B. Bhisitkul, D. S. Boyer, S. R. Sadda, and K. Zhang, “Seven-Year Outcomes in Ranibizumab-Treated Patients in ANCHOR, MARINA, and HORIZON: A Multicenter Cohort Study (SEVEN-UP),” Ophthalmology 120(11), 2292–2299 (2013).
[Crossref] [PubMed]

Schiöth, H. B.

A. Ringholm, R. Fredriksson, N. Poliakova, Y.-L. Yan, J. H. Postlethwait, D. Larhammar, and H. B. Schiöth, “One melanocortin 4 and two melanocortin 5 receptors from zebrafish show remarkable conservation in structure and pharmacology,” J. Neurochem. 82(1), 6–18 (2002).
[Crossref] [PubMed]

Schuman, J. S.

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

Schwartz, S. G.

J. L. Kovach, S. G. Schwartz, H. W. Flynn, and I. U. Scott, “Anti-VEGF Treatment Strategies for Wet AMD,” J. Ophthalmol. 2012, 786870 (2012).
[Crossref] [PubMed]

Scott, A. W.

M. M. Sachdeva, A. Moshiri, H. A. Leder, and A. W. Scott, “Endophthalmitis following intravitreal injection of anti-VEGF agents: long-term outcomes and the identification of unusual micro-organisms,” J. Ophthalmic Inflamm. Infect. 6(1), 2 (2016).
[Crossref] [PubMed]

Scott, I. U.

J. L. Kovach, S. G. Schwartz, H. W. Flynn, and I. U. Scott, “Anti-VEGF Treatment Strategies for Wet AMD,” J. Ophthalmol. 2012, 786870 (2012).
[Crossref] [PubMed]

Shah, K. B.

K. B. Shah and D. P. Han, “Proliferative diabetic retinopathy,” Int. Ophthalmol. Clin. 44(4), 69–84 (2004).
[Crossref] [PubMed]

Simó, R.

R. Simó and C. Hernández, “Intravitreous anti-VEGF for diabetic retinopathy: hopes and fears for a new therapeutic strategy,” Diabetologia 51(9), 1574–1580 (2008).
[Crossref] [PubMed]

Spital, G.

B. Heimes, F. Gunnemann, M. Ziegler, M. Gutfleisch, G. Spital, D. Pauleikhoff, and A. Lommatzsch, “Compliance von Patienten mit altersabhängiger Makuladegeneration unter Anti-VEGF-Therapie:Analyse und Verbesserungsvorschläge,” Ophthalmologe 113(11), 925–932 (2016).
[Crossref] [PubMed]

Spitsbergen, J. M.

A. L. Menke, J. M. Spitsbergen, A. P. M. Wolterbeek, and R. A. Woutersen, “Normal anatomy and histology of the adult zebrafish,” Toxicol. Pathol. 39(5), 759–775 (2011).
[Crossref] [PubMed]

Stahl, A.

T. Wecker, C. Ehlken, A. Bühler, C. Lange, H. Agostini, D. Böhringer, and A. Stahl, “Five-year visual acuity outcomes and injection patterns in patients with pro-re-nata treatments for AMD, DME, RVO and myopic CNV,” Br. J. Ophthalmol. 101(3), 353–359 (2017).
[Crossref] [PubMed]

Steffensen, J. F.

Z. Cao, L. D. Jensen, P. Rouhi, K. Hosaka, T. Länne, J. F. Steffensen, E. Wahlberg, and Y. Cao, “Hypoxia-induced retinopathy model in adult zebrafish,” Nat. Protoc. 5(12), 1903–1910 (2010).
[Crossref] [PubMed]

Stinson, W. G.

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

Swanson, E. A.

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

Tadayoni, R.

R. Tadayoni, E. Vicaut, F. Devin, C. Creuzot-Garcher, J. P. Berrod, Y. Le Mer, J. F. Korobelnik, M. Aout, P. Massin, and A. Gaudric, “A randomized controlled trial of alleviated positioning after small macular hole surgery,” Ophthalmology 118(1), 150–155 (2011).
[Crossref] [PubMed]

Tao, Y. K.

R. M. DiCicco, B. A. Bell, C. Kaul, J. G. Hollyfield, B. Anand-Apte, B. D. Perkins, Y. K. Tao, and A. Yuan, “Retinal regeneration following OCT-guided laser injury in zebrafish,” Invest. Ophthalmol. Vis. Sci. 55(10), 6281–6288 (2014).
[Crossref] [PubMed]

Thurman, S. T.

Tittle, R. K.

J. Bibliowicz, R. K. Tittle, and J. M. Gross, “Toward a better understanding of human eye disease insights from the zebrafish, Danio rerio,” Prog. Mol. Biol. Transl. Sci. 100, 287–330 (2011).
[Crossref] [PubMed]

Tomany, S. C.

D. S. Friedman, B. J. O’Colmain, B. Muñoz, S. C. Tomany, C. McCarty, P. T. de Jong, B. Nemesure, P. Mitchell, and J. Kempen, “Prevalence of age-related macular degeneration in the United States,” Arch. Ophthalmol. 122(4), 564–572 (2004).
[Crossref] [PubMed]

Tomidokoro, A.

Torres-Vazquez, J.

Y. Alvarez, M. L. Cederlund, D. C. Cottell, B. R. Bill, S. C. Ekker, J. Torres-Vazquez, B. M. Weinstein, D. R. Hyde, T. S. Vihtelic, and B. N. Kennedy, “Genetic determinants of hyaloid and retinal vasculature in zebrafish,” BMC Dev. Biol. 7(1), 114 (2007).
[Crossref] [PubMed]

Verma, Y.

K. D. Rao, Y. Verma, H. Patel, and P. Gupta, “Non-invasive ophthalmic imaging of adult zebrafish eye using optical coherence tomography,” CURRENT SCIENCE-BANGALORE 90, 1506 (2006).

Vicaut, E.

R. Tadayoni, E. Vicaut, F. Devin, C. Creuzot-Garcher, J. P. Berrod, Y. Le Mer, J. F. Korobelnik, M. Aout, P. Massin, and A. Gaudric, “A randomized controlled trial of alleviated positioning after small macular hole surgery,” Ophthalmology 118(1), 150–155 (2011).
[Crossref] [PubMed]

Vihtelic, T. S.

Y. Alvarez, M. L. Cederlund, D. C. Cottell, B. R. Bill, S. C. Ekker, J. Torres-Vazquez, B. M. Weinstein, D. R. Hyde, T. S. Vihtelic, and B. N. Kennedy, “Genetic determinants of hyaloid and retinal vasculature in zebrafish,” BMC Dev. Biol. 7(1), 114 (2007).
[Crossref] [PubMed]

Wahlberg, E.

Z. Cao, L. D. Jensen, P. Rouhi, K. Hosaka, T. Länne, J. F. Steffensen, E. Wahlberg, and Y. Cao, “Hypoxia-induced retinopathy model in adult zebrafish,” Nat. Protoc. 5(12), 1903–1910 (2010).
[Crossref] [PubMed]

Wählby, C.

T. Y. Chang, C. Pardo-Martin, A. Allalou, C. Wählby, and M. F. Yanik, “Fully automated cellular-resolution vertebrate screening platform with parallel animal processing,” Lab Chip 12(4), 711–716 (2012).
[Crossref] [PubMed]

Wang, R. K.

Wang, Z.

Wecker, T.

T. Wecker, C. Ehlken, A. Bühler, C. Lange, H. Agostini, D. Böhringer, and A. Stahl, “Five-year visual acuity outcomes and injection patterns in patients with pro-re-nata treatments for AMD, DME, RVO and myopic CNV,” Br. J. Ophthalmol. 101(3), 353–359 (2017).
[Crossref] [PubMed]

Weile, D. S.

D. S. Weile and E. Michielssen, “Genetic algorithm optimization applied to electromagnetics: a review,” IEEE Trans. Antenn. Propag. 45(3), 343–353 (1997).
[Crossref]

Weinstein, B. M.

Y. Alvarez, M. L. Cederlund, D. C. Cottell, B. R. Bill, S. C. Ekker, J. Torres-Vazquez, B. M. Weinstein, D. R. Hyde, T. S. Vihtelic, and B. N. Kennedy, “Genetic determinants of hyaloid and retinal vasculature in zebrafish,” BMC Dev. Biol. 7(1), 114 (2007).
[Crossref] [PubMed]

S. Isogai, M. Horiguchi, and B. M. Weinstein, “The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development,” Dev. Biol. 230(2), 278–301 (2001).
[Crossref] [PubMed]

Wittenborn, J. S.

D. B. Rein, J. S. Wittenborn, X. Zhang, A. A. Honeycutt, S. B. Lesesne, and J. Saaddine, “Forecasting age-related macular degeneration through the year 2050: The potential impact of new treatments,” Arch. Ophthalmol. 127(4), 533–540 (2009).
[Crossref] [PubMed]

Wolterbeek, A. P. M.

A. L. Menke, J. M. Spitsbergen, A. P. M. Wolterbeek, and R. A. Woutersen, “Normal anatomy and histology of the adult zebrafish,” Toxicol. Pathol. 39(5), 759–775 (2011).
[Crossref] [PubMed]

Woutersen, R. A.

A. L. Menke, J. M. Spitsbergen, A. P. M. Wolterbeek, and R. A. Woutersen, “Normal anatomy and histology of the adult zebrafish,” Toxicol. Pathol. 39(5), 759–775 (2011).
[Crossref] [PubMed]

Xie, J.

B. A. Bell, J. Xie, A. Yuan, C. Kaul, J. G. Hollyfield, and B. Anand-Apte, “Retinal Vasculature of Adult Zebrafish: In Vivo Imaging Using Confocal Scanning Laser Ophthalmoscopy,” Exp. Eye Res. 129, 107–118 (2014).
[Crossref] [PubMed]

Yan, Y.-L.

A. Ringholm, R. Fredriksson, N. Poliakova, Y.-L. Yan, J. H. Postlethwait, D. Larhammar, and H. B. Schiöth, “One melanocortin 4 and two melanocortin 5 receptors from zebrafish show remarkable conservation in structure and pharmacology,” J. Neurochem. 82(1), 6–18 (2002).
[Crossref] [PubMed]

Yang, Q.

Yanik, M. F.

T. Y. Chang, C. Pardo-Martin, A. Allalou, C. Wählby, and M. F. Yanik, “Fully automated cellular-resolution vertebrate screening platform with parallel animal processing,” Lab Chip 12(4), 711–716 (2012).
[Crossref] [PubMed]

Ying, G. S.

D. F. Martin, M. G. Maguire, G. S. Ying, J. E. Grunwald, S. L. Fine, and G. J. Jaffe, “Ranibizumab and Bevacizumab for Neovascular Age-Related Macular Degeneration,” N. Engl. J. Med. 364(20), 1897–1908 (2011).
[Crossref] [PubMed]

Yoshimura, N.

Yuan, A.

B. A. Bell, A. Yuan, R. M. Dicicco, J. Fogerty, E. M. Lessieur, and B. D. Perkins, “The adult zebrafish retina: In vivo optical sectioning with Confocal Scanning Laser Ophthalmoscopy and Spectral-Domain Optical Coherence Tomography,” Exp. Eye Res. 153, 65–78 (2016).
[Crossref] [PubMed]

R. M. DiCicco, B. A. Bell, C. Kaul, J. G. Hollyfield, B. Anand-Apte, B. D. Perkins, Y. K. Tao, and A. Yuan, “Retinal regeneration following OCT-guided laser injury in zebrafish,” Invest. Ophthalmol. Vis. Sci. 55(10), 6281–6288 (2014).
[Crossref] [PubMed]

B. A. Bell, J. Xie, A. Yuan, C. Kaul, J. G. Hollyfield, and B. Anand-Apte, “Retinal Vasculature of Adult Zebrafish: In Vivo Imaging Using Confocal Scanning Laser Ophthalmoscopy,” Exp. Eye Res. 129, 107–118 (2014).
[Crossref] [PubMed]

Zhang, K.

S. Rofagha, R. B. Bhisitkul, D. S. Boyer, S. R. Sadda, and K. Zhang, “Seven-Year Outcomes in Ranibizumab-Treated Patients in ANCHOR, MARINA, and HORIZON: A Multicenter Cohort Study (SEVEN-UP),” Ophthalmology 120(11), 2292–2299 (2013).
[Crossref] [PubMed]

Zhang, Q.

Zhang, X.

D. B. Rein, J. S. Wittenborn, X. Zhang, A. A. Honeycutt, S. B. Lesesne, and J. Saaddine, “Forecasting age-related macular degeneration through the year 2050: The potential impact of new treatments,” Arch. Ophthalmol. 127(4), 533–540 (2009).
[Crossref] [PubMed]

Ziegler, M.

B. Heimes, F. Gunnemann, M. Ziegler, M. Gutfleisch, G. Spital, D. Pauleikhoff, and A. Lommatzsch, “Compliance von Patienten mit altersabhängiger Makuladegeneration unter Anti-VEGF-Therapie:Analyse und Verbesserungsvorschläge,” Ophthalmologe 113(11), 925–932 (2016).
[Crossref] [PubMed]

Zon, L. I.

L. I. Zon and R. T. Peterson, “In vivo drug discovery in the zebrafish,” Nat. Rev. Drug Discov. 4(1), 35–44 (2005).
[Crossref] [PubMed]

Arch. Ophthalmol. (2)

D. B. Rein, J. S. Wittenborn, X. Zhang, A. A. Honeycutt, S. B. Lesesne, and J. Saaddine, “Forecasting age-related macular degeneration through the year 2050: The potential impact of new treatments,” Arch. Ophthalmol. 127(4), 533–540 (2009).
[Crossref] [PubMed]

D. S. Friedman, B. J. O’Colmain, B. Muñoz, S. C. Tomany, C. McCarty, P. T. de Jong, B. Nemesure, P. Mitchell, and J. Kempen, “Prevalence of age-related macular degeneration in the United States,” Arch. Ophthalmol. 122(4), 564–572 (2004).
[Crossref] [PubMed]

Biomed. Opt. Express (1)

BMC Dev. Biol. (1)

Y. Alvarez, M. L. Cederlund, D. C. Cottell, B. R. Bill, S. C. Ekker, J. Torres-Vazquez, B. M. Weinstein, D. R. Hyde, T. S. Vihtelic, and B. N. Kennedy, “Genetic determinants of hyaloid and retinal vasculature in zebrafish,” BMC Dev. Biol. 7(1), 114 (2007).
[Crossref] [PubMed]

Br. J. Ophthalmol. (1)

T. Wecker, C. Ehlken, A. Bühler, C. Lange, H. Agostini, D. Böhringer, and A. Stahl, “Five-year visual acuity outcomes and injection patterns in patients with pro-re-nata treatments for AMD, DME, RVO and myopic CNV,” Br. J. Ophthalmol. 101(3), 353–359 (2017).
[Crossref] [PubMed]

Curr. Opin. Drug Discov. Devel. (1)

A. L. Rubinstein, “Zebrafish: from disease modeling to drug discovery,” Curr. Opin. Drug Discov. Devel. 6(2), 218–223 (2003).
[PubMed]

Curr. Opin. Pharmacol. (1)

P. Goldsmith, “Zebrafish as a pharmacological tool: the how, why and when,” Curr. Opin. Pharmacol. 4(5), 504–512 (2004).
[Crossref] [PubMed]

CURRENT SCIENCE-BANGALORE (1)

K. D. Rao, Y. Verma, H. Patel, and P. Gupta, “Non-invasive ophthalmic imaging of adult zebrafish eye using optical coherence tomography,” CURRENT SCIENCE-BANGALORE 90, 1506 (2006).

Dev. Biol. (1)

S. Isogai, M. Horiguchi, and B. M. Weinstein, “The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development,” Dev. Biol. 230(2), 278–301 (2001).
[Crossref] [PubMed]

Diabetologia (1)

R. Simó and C. Hernández, “Intravitreous anti-VEGF for diabetic retinopathy: hopes and fears for a new therapeutic strategy,” Diabetologia 51(9), 1574–1580 (2008).
[Crossref] [PubMed]

Exp. Eye Res. (2)

B. A. Bell, J. Xie, A. Yuan, C. Kaul, J. G. Hollyfield, and B. Anand-Apte, “Retinal Vasculature of Adult Zebrafish: In Vivo Imaging Using Confocal Scanning Laser Ophthalmoscopy,” Exp. Eye Res. 129, 107–118 (2014).
[Crossref] [PubMed]

B. A. Bell, A. Yuan, R. M. Dicicco, J. Fogerty, E. M. Lessieur, and B. D. Perkins, “The adult zebrafish retina: In vivo optical sectioning with Confocal Scanning Laser Ophthalmoscopy and Spectral-Domain Optical Coherence Tomography,” Exp. Eye Res. 153, 65–78 (2016).
[Crossref] [PubMed]

Eye (Lond.) (2)

J. Chhetri, G. Jacobson, and N. Gueven, “Zebrafishon the move towards ophthalmological research,” Eye (Lond.) 28(4), 367–380 (2014).
[Crossref] [PubMed]

K. G. Falavarjani and Q. D. Nguyen, “Adverse events and complications associated with intravitreal injection of anti-VEGF agents: a review of literature,” Eye (Lond.) 27(7), 787–794 (2013).
[Crossref] [PubMed]

IEEE Trans. Antenn. Propag. (1)

D. S. Weile and E. Michielssen, “Genetic algorithm optimization applied to electromagnetics: a review,” IEEE Trans. Antenn. Propag. 45(3), 343–353 (1997).
[Crossref]

IEEE Trans. Image Process. (1)

S. Chen and R. M. Haralick, “Recursive erosion, dilation, opening, and closing transforms,” IEEE Trans. Image Process. 4(3), 335–345 (1995).
[Crossref] [PubMed]

Int. Ophthalmol. Clin. (1)

K. B. Shah and D. P. Han, “Proliferative diabetic retinopathy,” Int. Ophthalmol. Clin. 44(4), 69–84 (2004).
[Crossref] [PubMed]

Invest. Ophthalmol. Vis. Sci. (1)

R. M. DiCicco, B. A. Bell, C. Kaul, J. G. Hollyfield, B. Anand-Apte, B. D. Perkins, Y. K. Tao, and A. Yuan, “Retinal regeneration following OCT-guided laser injury in zebrafish,” Invest. Ophthalmol. Vis. Sci. 55(10), 6281–6288 (2014).
[Crossref] [PubMed]

J. Neurochem. (1)

A. Ringholm, R. Fredriksson, N. Poliakova, Y.-L. Yan, J. H. Postlethwait, D. Larhammar, and H. B. Schiöth, “One melanocortin 4 and two melanocortin 5 receptors from zebrafish show remarkable conservation in structure and pharmacology,” J. Neurochem. 82(1), 6–18 (2002).
[Crossref] [PubMed]

J. Ophthalmic Inflamm. Infect. (1)

M. M. Sachdeva, A. Moshiri, H. A. Leder, and A. W. Scott, “Endophthalmitis following intravitreal injection of anti-VEGF agents: long-term outcomes and the identification of unusual micro-organisms,” J. Ophthalmic Inflamm. Infect. 6(1), 2 (2016).
[Crossref] [PubMed]

J. Ophthalmol. (1)

J. L. Kovach, S. G. Schwartz, H. W. Flynn, and I. U. Scott, “Anti-VEGF Treatment Strategies for Wet AMD,” J. Ophthalmol. 2012, 786870 (2012).
[Crossref] [PubMed]

Lab Chip (1)

T. Y. Chang, C. Pardo-Martin, A. Allalou, C. Wählby, and M. F. Yanik, “Fully automated cellular-resolution vertebrate screening platform with parallel animal processing,” Lab Chip 12(4), 711–716 (2012).
[Crossref] [PubMed]

N. Engl. J. Med. (2)

E. S. Gragoudas, A. P. Adamis, E. T. Cunningham, M. Feinsod, and D. R. Guyer, “Pegaptanib for neovascular age-related macular degeneration,” N. Engl. J. Med. 351(27), 2805–2816 (2004).
[Crossref] [PubMed]

D. F. Martin, M. G. Maguire, G. S. Ying, J. E. Grunwald, S. L. Fine, and G. J. Jaffe, “Ranibizumab and Bevacizumab for Neovascular Age-Related Macular Degeneration,” N. Engl. J. Med. 364(20), 1897–1908 (2011).
[Crossref] [PubMed]

Nat. Protoc. (1)

Z. Cao, L. D. Jensen, P. Rouhi, K. Hosaka, T. Länne, J. F. Steffensen, E. Wahlberg, and Y. Cao, “Hypoxia-induced retinopathy model in adult zebrafish,” Nat. Protoc. 5(12), 1903–1910 (2010).
[Crossref] [PubMed]

Nat. Rev. Drug Discov. (2)

C. A. MacRae and R. T. Peterson, “Zebrafish as tools for drug discovery,” Nat. Rev. Drug Discov. 14(10), 721–731 (2015).
[Crossref] [PubMed]

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Figures (10)

Fig. 1
Fig. 1 In vivo retinal OCT imaging in zebrafish. (a) Custom-built SD-OCT system. CMOS, detector; f, collimating, objective, ophthalmic, and scan lenses; G, galvanometers; M, mirror; PC, polarization controller; SLD, superluminescent diode; VPHG, volume phase holograph grating. (b) Zebrafish retina was imaged in air through a contact lens and positioned using a custom holder (inset) on a 5-axis alignment stage.
Fig. 2
Fig. 2 Block diagram showing vessel segmentation, labeling, and feature extraction steps for automated vascular biometry.
Fig. 3
Fig. 3 Branch kernel matrix. 18 predefined 3x3 pixel kernels were created to represent all possible vessel branch orientations.
Fig. 4
Fig. 4 Quantitative vascular biometry. Length, curvature, and angle were defined using skeletonized vascular maps. Branch generations were assigned based on their connectivity relative to the ONH.
Fig. 5
Fig. 5 In vivo retinal OCT in zebrafish. (a) En face OCT projection with representative orthogonal cross-sections (blue/red lines and insets). (b) 5-frame averaged OCT cross-section with labeled retinal layers. GCL, ganglion cell layer; IPL, inner plexiform layer; INL, inner nuclear layer; OPL, outer plexiform layer; ONL, outer nuclear layer; OS, outer segment; and RPE, retinal pigment epithelium.
Fig. 6
Fig. 6 In vivo retinal OCT-A in zebrafish. (a) En face OCT-A projection with representative orthogonal cross-sections (blue/red lines and insets) showing retinal vessels (arrow) and RPE artifacts. (b) OCT-A projection with corresponding segmentation mask overlay. Vessel branches are color-coded based on their branch generation relative to the ONH (white circle). Scale bar 1°.
Fig. 7
Fig. 7 Segmentation errors at the FOV periphery. Representative en face (a), (d) OCT; (b), (e) OCT-A; and (c), (f) segmentation maps of the same eye at two longitudinal timepoints. Some generation 3 branches were misidentified as part of generation 2 branches because of poor OCT-A contrast (pink arrows). Similarly, branches cropped by the edge of the FOV (dashed lines) with sufficient contrast may be misidentified as part of the preceding generation (orange arrows).
Fig. 8
Fig. 8 Segmentation errors at the ONH. (a)-(c) En face OCT-A, (d)-(f) segmentation maps, and (g)-(i) magnified views around the ONH of the same eye at three longitudinal timepoints. (d), (g) Correctly labeled data sets show ONH vessels in gray. (e), (h) and (f), (i) Branch generation labeling errors show ONH vessels labeled as first-generation vessels (arrows).
Fig. 9
Fig. 9 Quantitative vascular biometry. Vessel branch (a) length, (b) curvature, and (c) angle of 10 repeated longitudinal data sets (columns) for both eyes of 10 zebrafish (column groups). Each column group showed biometric changes in 10 imaging sessions for one eye. Biometrics in each eye were grouped by branch generation (row groups) and each row in generation represent one vessel in the respective generation. Color coded biometric features shows change in length, curvature, and angle in each vessel over time.
Fig. 10
Fig. 10 Vessel branch length comparison in the same eye between longitudinal timepoints. (a) Representative biometric map showing vessel branch length differences (columns) between 10 repeated data sets (rows) in one eye. (b)-(d) Segmented vascular maps at 3 representative timepoints showing similar length parameters in the first and second vessel generations and increased variability in higher generations as a result of FOV differences (arrow and asterisks).

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