Abstract

We demonstrate the repeatability of lamina cribrosa (LC) microarchitecture for in vivo 3D optical coherence tomography (OCT) scans of healthy, glaucoma suspects, and glaucomatous eyes. Eyes underwent two scans using a prototype adaptive optics spectral domain OCT (AO-SDOCT) device from which LC microarchitecture was semi-automatically segmented. LC segmentations were used to quantify pore and beam structure through several global microarchitecture parameters. Repeatability of LC microarchitecture was assessed qualitatively and quantitatively by calculating parameter imprecision. For all but one parameters (pore volume) measurement imprecision was <4.7% of the mean value, indicating good measurement reproducibility. Imprecision ranged between 27.3% and 54.5% of the population standard deviation for each parameter, while there was not a significant effect on imprecision due to disease status, indicating utility in testing for LC structural trends.

© 2014 Optical Society of America

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2014 (1)

A. J. Tatham, A. Miki, R. N. Weinreb, L. M. Zangwill, and F. A. Medeiros, “Defects of the lamina cribrosa in eyes with localized retinal nerve fiber layer loss,” Ophthalmology121, 110–118 (2014).
[PubMed]

2013 (3)

2012 (6)

D. X. Hammer, R. D. Ferguson, M. Mujat, A. Patel, E. Plumb, N. Iftimia, T. Y. P. Chui, J. D. Akula, and A. B. Fulton, “Multimodal adaptive optics retinal imager: design and performance,” J. Opt. Soc. Am. A29(12), 2598–2607 (2012).
[CrossRef] [PubMed]

T. Akagi, M. Hangai, K. Takayama, A. Nonaka, S. Ooto, and N. Yoshimura, “In vivo imaging of lamina cribrosa pores by adaptive optics scanning laser ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci.53(7), 4111–4119 (2012).
[CrossRef] [PubMed]

H.-Y. L. Park, S. H. Jeon, and C. K. Park, “Enhanced depth imaging detects lamina cribrosa thickness differences in normal tension glaucoma and primary open-angle glaucoma,” Ophthalmology119(1), 10–20 (2012).
[CrossRef] [PubMed]

S. Kiumehr, S. C. Park, D. Syril, C. C. Teng, C. Tello, J. M. Liebmann, and R. Ritch, “In vivo evaluation of focal lamina cribrosa defects in glaucoma,” Arch. Ophthalmol.130(5), 552–559 (2012).
[PubMed]

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods9(7), 676–682 (2012).
[CrossRef] [PubMed]

R. Rezakhaniha, A. Agianniotis, J. T. C. Schrauwen, A. Griffa, D. Sage, C. V. C. Bouten, F. N. van de Vosse, M. Unser, and N. Stergiopulos, “Experimental investigation of collagen waviness and orientation in the arterial adventitia using confocal laser scanning microscopy,” Biomech. Model. Mechanobiol.11(3-4), 461–473 (2012).
[CrossRef] [PubMed]

2011 (3)

R. Grytz, G. Meschke, and J. B. Jonas, “The collagen fibril architecture in the lamina cribrosa and peripapillary sclera predicted by a computational remodeling approach,” Biomech. Model. Mechanobiol.10(3), 371–382 (2011).
[CrossRef] [PubMed]

E. J. Lee, T.-W. Kim, R. N. Weinreb, K. H. Park, S. H. Kim, and D. M. Kim, “Visualization of the lamina cribrosa using enhanced depth imaging spectral-domain optical coherence tomography,” Am. J. Ophthalmology152(1), 87–95 (2011).

K. M. Ivers, C. Li, N. Patel, N. Sredar, X. Luo, H. Queener, R. S. Harwerth, and J. Porter, “Reproducibility of measuring lamina cribrosa pore geometry in human and nonhuman primates with in vivo adaptive optics imaging,” Invest. Ophthalmol. Vis. Sci.52(8), 5473–5480 (2011).
[CrossRef] [PubMed]

2010 (6)

N. G. Strouthidis, S. Demirel, R. Asaoka, C. Cossio-Zuniga, and D. F. Garway-Heath, “The Heidelberg retina tomograph Glaucoma Probability Score: reproducibility and measurement of progression,” Ophthalmology117(4), 724–729 (2010).
[CrossRef] [PubMed]

C. Alexandrescu, A. M. Dascalu, A. Panca, A. Sescioreanu, C. Mitulescu, R. Ciuluvica, L. Voinea, and C. Celea, “Confocal scanning laser ophthalmoscopy in glaucoma diagnosis and management,” J. Med. Life3(3), 229–234 (2010).
[PubMed]

C. K. S. Leung, S. Lam, R. N. Weinreb, S. Liu, C. Ye, L. Liu, J. He, G. W. K. Lai, T. Li, and D. S. Lam, “Retinal nerve fiber layer imaging with spectral-domain optical coherence tomography: analysis of the retinal nerve fiber layer map for glaucoma detection,” Ophthalmology117(9), 1684–1691 (2010).
[CrossRef] [PubMed]

M. Doube, M. M. Kłosowski, I. Arganda-Carreras, F. P. Cordelières, R. P. Dougherty, J. S. Jackson, B. Schmid, J. R. Hutchinson, and S. J. Shefelbine, “BoneJ: Free and extensible bone image analysis in ImageJ,” Bone47(6), 1076–1079 (2010).
[CrossRef] [PubMed]

M. Winkler, B. Jester, C. Nien-Shy, S. Massei, D. S. Minckler, J. V. Jester, and D. J. Brown, “High resolution three-dimensional reconstruction of the collagenous matrix of the human optic nerve head,” Brain Res. Bull.81(2-3), 339–348 (2010).
[CrossRef] [PubMed]

I. A. Sigal, J. G. Flanagan, I. Tertinegg, and C. R. Ethier, “3D morphometry of the human optic nerve head,” Exp. Eye Res.90(1), 70–80 (2010).
[CrossRef] [PubMed]

2009 (4)

R. J. Zawadzki, S. S. Choi, A. R. Fuller, J. W. Evans, B. Hamann, and J. S. Werner, “Cellular resolution volumetric in vivo retinal imaging with adaptive optics–optical coherence tomography,” Opt. Express17(5), 4084–4094 (2009).

C. Torti, B. Povazay, B. Hofer, A. Unterhuber, J. Carroll, P. K. Ahnelt, and W. Drexler, “Adaptive optics optical coherence tomography at 120,000 depth scans/s for non-invasive cellular phenotyping of the living human retina,” Opt. Express17(22), 19382–19400 (2009).
[CrossRef] [PubMed]

O. Tan, V. Chopra, A. T.-H. Lu, J. S. Schuman, H. Ishikawa, G. Wollstein, R. Varma, and D. Huang, “Detection of macular ganglion cell loss in glaucoma by Fourier-domain optical coherence tomography,” Ophthalmology116(12), 2305 (2009).

K. A. Townsend, G. Wollstein, and J. S. Schuman, “Imaging of the retinal nerve fibre layer for glaucoma,” Br. J. Ophthalmol.93(2), 139–143 (2009).
[CrossRef] [PubMed]

2008 (3)

O. Tan, G. Li, A. T.-H. Lu, R. Varma, D. Huang, and Advanced Imaging for Glaucoma Study Group, “Mapping of macular substructures with optical coherence tomography for glaucoma diagnosis,” Ophthalmology115(6), 949–956 (2008).
[CrossRef] [PubMed]

J. W. Bartlett and C. Frost, “Reliability, repeatability and reproducibility: analysis of measurement errors in continuous variables,” Ultrasound Obstet. Gynecol.31(4), 466–475 (2008).
[CrossRef] [PubMed]

M. D. Roberts, V. Grau, J. Grimm, J. Reynaud, A. J. Bellezza, C. F. Burgoyne, and J. C. Downs, “Remodeling of the connective tissue microarchitecture of the lamina cribrosa in early experimental glaucoma,” Invest. Ophthalmol. Vis. Sci.50(2), 681–690 (2008).
[CrossRef] [PubMed]

2007 (1)

2006 (2)

H. A. Quigley and A. T. Broman, “The number of people with glaucoma worldwide in 2010 and 2020,” Br. J. Ophthalmol.90(3), 262–267 (2006).
[CrossRef] [PubMed]

D. Ng, L. M. Zangwill, L. Racette, C. Bowd, J. P. Pascual, R. R. A. Bourne, C. Boden, R. N. Weinreb, and P. A. Sample, “Agreement and repeatability for standard automated perimetry and confocal scanning laser ophthalmoscopy in the diagnostic innovations in glaucoma study,” Am. J. Ophthalmol.142(3), 381–386 (2006).
[CrossRef] [PubMed]

2005 (3)

H. A. Quigley, “Glaucoma: macrocosm to microcosm the Friedenwald lecture,” Invest. Ophthalmol. Vis. Sci.46(8), 2663–2670 (2005).
[CrossRef] [PubMed]

G. Wollstein, H. Ishikawa, J. Wang, S. A. Beaton, and J. S. Schuman, “Comparison of three optical coherence tomography scanning areas for detection of glaucomatous damage,” Am. J. Ophthalmol.139(1), 39–43 (2005).
[CrossRef] [PubMed]

F. A. Medeiros, L. M. Zangwill, C. Bowd, R. M. Vessani, R. Susanna, and R. N. Weinreb, “Evaluation of retinal nerve fiber layer, optic nerve head, and macular thickness measurements for glaucoma detection using optical coherence tomography,” Am. J. Ophthalmol.139(1), 44–55 (2005).
[CrossRef] [PubMed]

2004 (1)

G. Tezel, K. Trinkaus, and M. B. Wax, “Alterations in the morphology of lamina cribrosa pores in glaucomatous eyes,” Br. J. Ophthalmol.88(2), 251–256 (2004).
[CrossRef] [PubMed]

1998 (1)

L. Fontana, A. Bhandari, F. W. Fitzke, and R. A. Hitchings, “In vivo morphometry of the lamina cribrosa and its relation to visual field loss in glaucoma,” Curr. Eye Res.17(4), 363–369 (1998).
[CrossRef] [PubMed]

1990 (1)

L. Dandona, H. A. Quigley, A. E. Brown, and C. Enger, “Quantitative regional structure of the normal human lamina cribrosa. A racial comparison,” Arch. Ophthalmol.108(3), 393–398 (1990).
[CrossRef] [PubMed]

1986 (1)

J. M. Bland and D. G. Altman, “Statistical methods for assessing agreement between two methods of clinical measurement,” Lancet327(8476), 307–310 (1986).
[CrossRef] [PubMed]

1984 (1)

T. Y. Zhang and C. Y. Suen, “A fast parallel algorithm for thinning digital patterns,” Commun. ACM27(3), 236–239 (1984).

1981 (1)

H. A. Quigley and E. M. Addicks, “Regional differences in the structure of the lamina cribrosa and their relation to glaucomatous optic nerve damage,” Arch. Ophthalmol.99(1), 137–143 (1981).
[CrossRef] [PubMed]

Addicks, E. M.

H. A. Quigley and E. M. Addicks, “Regional differences in the structure of the lamina cribrosa and their relation to glaucomatous optic nerve damage,” Arch. Ophthalmol.99(1), 137–143 (1981).
[CrossRef] [PubMed]

Agianniotis, A.

R. Rezakhaniha, A. Agianniotis, J. T. C. Schrauwen, A. Griffa, D. Sage, C. V. C. Bouten, F. N. van de Vosse, M. Unser, and N. Stergiopulos, “Experimental investigation of collagen waviness and orientation in the arterial adventitia using confocal laser scanning microscopy,” Biomech. Model. Mechanobiol.11(3-4), 461–473 (2012).
[CrossRef] [PubMed]

Ahnelt, P. K.

Akagi, T.

T. Akagi, M. Hangai, K. Takayama, A. Nonaka, S. Ooto, and N. Yoshimura, “In vivo imaging of lamina cribrosa pores by adaptive optics scanning laser ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci.53(7), 4111–4119 (2012).
[CrossRef] [PubMed]

Akula, J. D.

Alexandrescu, C.

C. Alexandrescu, A. M. Dascalu, A. Panca, A. Sescioreanu, C. Mitulescu, R. Ciuluvica, L. Voinea, and C. Celea, “Confocal scanning laser ophthalmoscopy in glaucoma diagnosis and management,” J. Med. Life3(3), 229–234 (2010).
[PubMed]

Altman, D. G.

J. M. Bland and D. G. Altman, “Statistical methods for assessing agreement between two methods of clinical measurement,” Lancet327(8476), 307–310 (1986).
[CrossRef] [PubMed]

Arganda-Carreras, I.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods9(7), 676–682 (2012).
[CrossRef] [PubMed]

M. Doube, M. M. Kłosowski, I. Arganda-Carreras, F. P. Cordelières, R. P. Dougherty, J. S. Jackson, B. Schmid, J. R. Hutchinson, and S. J. Shefelbine, “BoneJ: Free and extensible bone image analysis in ImageJ,” Bone47(6), 1076–1079 (2010).
[CrossRef] [PubMed]

Asaoka, R.

N. G. Strouthidis, S. Demirel, R. Asaoka, C. Cossio-Zuniga, and D. F. Garway-Heath, “The Heidelberg retina tomograph Glaucoma Probability Score: reproducibility and measurement of progression,” Ophthalmology117(4), 724–729 (2010).
[CrossRef] [PubMed]

Bartlett, J. W.

J. W. Bartlett and C. Frost, “Reliability, repeatability and reproducibility: analysis of measurement errors in continuous variables,” Ultrasound Obstet. Gynecol.31(4), 466–475 (2008).
[CrossRef] [PubMed]

Beaton, S. A.

G. Wollstein, H. Ishikawa, J. Wang, S. A. Beaton, and J. S. Schuman, “Comparison of three optical coherence tomography scanning areas for detection of glaucomatous damage,” Am. J. Ophthalmol.139(1), 39–43 (2005).
[CrossRef] [PubMed]

Bellezza, A. J.

M. D. Roberts, V. Grau, J. Grimm, J. Reynaud, A. J. Bellezza, C. F. Burgoyne, and J. C. Downs, “Remodeling of the connective tissue microarchitecture of the lamina cribrosa in early experimental glaucoma,” Invest. Ophthalmol. Vis. Sci.50(2), 681–690 (2008).
[CrossRef] [PubMed]

Bhandari, A.

L. Fontana, A. Bhandari, F. W. Fitzke, and R. A. Hitchings, “In vivo morphometry of the lamina cribrosa and its relation to visual field loss in glaucoma,” Curr. Eye Res.17(4), 363–369 (1998).
[CrossRef] [PubMed]

Bilonick, R. A.

B. Wang, J. E. Nevins, Z. Nadler, G. Wollstein, H. Ishikawa, R. A. Bilonick, L. Kagemann, I. A. Sigal, I. Grulkowski, J. J. Liu, M. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “In vivo lamina cribrosa micro-architecture in healthy and glaucomatous eyes as assessed by optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.54(13), 8270–8274 (2013).
[CrossRef] [PubMed]

Bland, J. M.

J. M. Bland and D. G. Altman, “Statistical methods for assessing agreement between two methods of clinical measurement,” Lancet327(8476), 307–310 (1986).
[CrossRef] [PubMed]

Boden, C.

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M. Winkler, B. Jester, C. Nien-Shy, S. Massei, D. S. Minckler, J. V. Jester, and D. J. Brown, “High resolution three-dimensional reconstruction of the collagenous matrix of the human optic nerve head,” Brain Res. Bull.81(2-3), 339–348 (2010).
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Celea, C.

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Chopra, V.

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Chui, T. Y. P.

Ciuluvica, R.

C. Alexandrescu, A. M. Dascalu, A. Panca, A. Sescioreanu, C. Mitulescu, R. Ciuluvica, L. Voinea, and C. Celea, “Confocal scanning laser ophthalmoscopy in glaucoma diagnosis and management,” J. Med. Life3(3), 229–234 (2010).
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M. D. Roberts, V. Grau, J. Grimm, J. Reynaud, A. J. Bellezza, C. F. Burgoyne, and J. C. Downs, “Remodeling of the connective tissue microarchitecture of the lamina cribrosa in early experimental glaucoma,” Invest. Ophthalmol. Vis. Sci.50(2), 681–690 (2008).
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Eliceiri, K.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods9(7), 676–682 (2012).
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L. Dandona, H. A. Quigley, A. E. Brown, and C. Enger, “Quantitative regional structure of the normal human lamina cribrosa. A racial comparison,” Arch. Ophthalmol.108(3), 393–398 (1990).
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Ferguson, R. D.

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Frise, E.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods9(7), 676–682 (2012).
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Fuller, A. R.

Fulton, A. B.

Garway-Heath, D. F.

N. G. Strouthidis, S. Demirel, R. Asaoka, C. Cossio-Zuniga, and D. F. Garway-Heath, “The Heidelberg retina tomograph Glaucoma Probability Score: reproducibility and measurement of progression,” Ophthalmology117(4), 724–729 (2010).
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M. D. Roberts, V. Grau, J. Grimm, J. Reynaud, A. J. Bellezza, C. F. Burgoyne, and J. C. Downs, “Remodeling of the connective tissue microarchitecture of the lamina cribrosa in early experimental glaucoma,” Invest. Ophthalmol. Vis. Sci.50(2), 681–690 (2008).
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Griffa, A.

R. Rezakhaniha, A. Agianniotis, J. T. C. Schrauwen, A. Griffa, D. Sage, C. V. C. Bouten, F. N. van de Vosse, M. Unser, and N. Stergiopulos, “Experimental investigation of collagen waviness and orientation in the arterial adventitia using confocal laser scanning microscopy,” Biomech. Model. Mechanobiol.11(3-4), 461–473 (2012).
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M. D. Roberts, V. Grau, J. Grimm, J. Reynaud, A. J. Bellezza, C. F. Burgoyne, and J. C. Downs, “Remodeling of the connective tissue microarchitecture of the lamina cribrosa in early experimental glaucoma,” Invest. Ophthalmol. Vis. Sci.50(2), 681–690 (2008).
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Z. Nadler, B. Wang, G. Wollstein, J. E. Nevins, H. Ishikawa, L. Kagemann, I. A. Sigal, R. D. Ferguson, D. X. Hammer, I. Grulkowski, J. J. Liu, M. F. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “Automated lamina cribrosa microstructural segmentation in optical coherence tomography scans of healthy and glaucomatous eyes,” Biomed. Opt. Express4(11), 2596–2608 (2013).

B. Wang, J. E. Nevins, Z. Nadler, G. Wollstein, H. Ishikawa, R. A. Bilonick, L. Kagemann, I. A. Sigal, I. Grulkowski, J. J. Liu, M. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “In vivo lamina cribrosa micro-architecture in healthy and glaucomatous eyes as assessed by optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.54(13), 8270–8274 (2013).
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R. Grytz, G. Meschke, and J. B. Jonas, “The collagen fibril architecture in the lamina cribrosa and peripapillary sclera predicted by a computational remodeling approach,” Biomech. Model. Mechanobiol.10(3), 371–382 (2011).
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Hammer, D. X.

Hangai, M.

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K. M. Ivers, C. Li, N. Patel, N. Sredar, X. Luo, H. Queener, R. S. Harwerth, and J. Porter, “Reproducibility of measuring lamina cribrosa pore geometry in human and nonhuman primates with in vivo adaptive optics imaging,” Invest. Ophthalmol. Vis. Sci.52(8), 5473–5480 (2011).
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A. S. Vilupuru, N. V. Rangaswamy, L. J. Frishman, E. L. Smith, R. S. Harwerth, and A. Roorda, “Adaptive optics scanning laser ophthalmoscopy for in vivo imaging of lamina cribrosa,” J. Opt. Soc. Am. A24(5), 1417–1425 (2007).
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C. K. S. Leung, S. Lam, R. N. Weinreb, S. Liu, C. Ye, L. Liu, J. He, G. W. K. Lai, T. Li, and D. S. Lam, “Retinal nerve fiber layer imaging with spectral-domain optical coherence tomography: analysis of the retinal nerve fiber layer map for glaucoma detection,” Ophthalmology117(9), 1684–1691 (2010).
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Hitchings, R. A.

L. Fontana, A. Bhandari, F. W. Fitzke, and R. A. Hitchings, “In vivo morphometry of the lamina cribrosa and its relation to visual field loss in glaucoma,” Curr. Eye Res.17(4), 363–369 (1998).
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Hofer, B.

Hornegger, J.

B. Wang, J. E. Nevins, Z. Nadler, G. Wollstein, H. Ishikawa, R. A. Bilonick, L. Kagemann, I. A. Sigal, I. Grulkowski, J. J. Liu, M. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “In vivo lamina cribrosa micro-architecture in healthy and glaucomatous eyes as assessed by optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.54(13), 8270–8274 (2013).
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Z. Nadler, B. Wang, G. Wollstein, J. E. Nevins, H. Ishikawa, L. Kagemann, I. A. Sigal, R. D. Ferguson, D. X. Hammer, I. Grulkowski, J. J. Liu, M. F. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “Automated lamina cribrosa microstructural segmentation in optical coherence tomography scans of healthy and glaucomatous eyes,” Biomed. Opt. Express4(11), 2596–2608 (2013).

Huang, D.

O. Tan, V. Chopra, A. T.-H. Lu, J. S. Schuman, H. Ishikawa, G. Wollstein, R. Varma, and D. Huang, “Detection of macular ganglion cell loss in glaucoma by Fourier-domain optical coherence tomography,” Ophthalmology116(12), 2305 (2009).

O. Tan, G. Li, A. T.-H. Lu, R. Varma, D. Huang, and Advanced Imaging for Glaucoma Study Group, “Mapping of macular substructures with optical coherence tomography for glaucoma diagnosis,” Ophthalmology115(6), 949–956 (2008).
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Iftimia, N.

Ishikawa, H.

B. Wang, J. E. Nevins, Z. Nadler, G. Wollstein, H. Ishikawa, R. A. Bilonick, L. Kagemann, I. A. Sigal, I. Grulkowski, J. J. Liu, M. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “In vivo lamina cribrosa micro-architecture in healthy and glaucomatous eyes as assessed by optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.54(13), 8270–8274 (2013).
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Z. Nadler, B. Wang, G. Wollstein, J. E. Nevins, H. Ishikawa, L. Kagemann, I. A. Sigal, R. D. Ferguson, D. X. Hammer, I. Grulkowski, J. J. Liu, M. F. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “Automated lamina cribrosa microstructural segmentation in optical coherence tomography scans of healthy and glaucomatous eyes,” Biomed. Opt. Express4(11), 2596–2608 (2013).

O. Tan, V. Chopra, A. T.-H. Lu, J. S. Schuman, H. Ishikawa, G. Wollstein, R. Varma, and D. Huang, “Detection of macular ganglion cell loss in glaucoma by Fourier-domain optical coherence tomography,” Ophthalmology116(12), 2305 (2009).

G. Wollstein, H. Ishikawa, J. Wang, S. A. Beaton, and J. S. Schuman, “Comparison of three optical coherence tomography scanning areas for detection of glaucomatous damage,” Am. J. Ophthalmol.139(1), 39–43 (2005).
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N. Sredar, K. M. Ivers, H. M. Queener, G. Zouridakis, and J. Porter, “3D modeling to characterize lamina cribrosa surface and pore geometries using in vivo images from normal and glaucomatous eyes,” Biomed. Opt. Express4(7), 1153–1165 (2013).
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K. M. Ivers, C. Li, N. Patel, N. Sredar, X. Luo, H. Queener, R. S. Harwerth, and J. Porter, “Reproducibility of measuring lamina cribrosa pore geometry in human and nonhuman primates with in vivo adaptive optics imaging,” Invest. Ophthalmol. Vis. Sci.52(8), 5473–5480 (2011).
[CrossRef] [PubMed]

Jackson, J. S.

M. Doube, M. M. Kłosowski, I. Arganda-Carreras, F. P. Cordelières, R. P. Dougherty, J. S. Jackson, B. Schmid, J. R. Hutchinson, and S. J. Shefelbine, “BoneJ: Free and extensible bone image analysis in ImageJ,” Bone47(6), 1076–1079 (2010).
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H.-Y. L. Park, S. H. Jeon, and C. K. Park, “Enhanced depth imaging detects lamina cribrosa thickness differences in normal tension glaucoma and primary open-angle glaucoma,” Ophthalmology119(1), 10–20 (2012).
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M. Winkler, B. Jester, C. Nien-Shy, S. Massei, D. S. Minckler, J. V. Jester, and D. J. Brown, “High resolution three-dimensional reconstruction of the collagenous matrix of the human optic nerve head,” Brain Res. Bull.81(2-3), 339–348 (2010).
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Jester, J. V.

M. Winkler, B. Jester, C. Nien-Shy, S. Massei, D. S. Minckler, J. V. Jester, and D. J. Brown, “High resolution three-dimensional reconstruction of the collagenous matrix of the human optic nerve head,” Brain Res. Bull.81(2-3), 339–348 (2010).
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Jonas, J. B.

R. Grytz, G. Meschke, and J. B. Jonas, “The collagen fibril architecture in the lamina cribrosa and peripapillary sclera predicted by a computational remodeling approach,” Biomech. Model. Mechanobiol.10(3), 371–382 (2011).
[CrossRef] [PubMed]

Kagemann, L.

B. Wang, J. E. Nevins, Z. Nadler, G. Wollstein, H. Ishikawa, R. A. Bilonick, L. Kagemann, I. A. Sigal, I. Grulkowski, J. J. Liu, M. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “In vivo lamina cribrosa micro-architecture in healthy and glaucomatous eyes as assessed by optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.54(13), 8270–8274 (2013).
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Z. Nadler, B. Wang, G. Wollstein, J. E. Nevins, H. Ishikawa, L. Kagemann, I. A. Sigal, R. D. Ferguson, D. X. Hammer, I. Grulkowski, J. J. Liu, M. F. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “Automated lamina cribrosa microstructural segmentation in optical coherence tomography scans of healthy and glaucomatous eyes,” Biomed. Opt. Express4(11), 2596–2608 (2013).

Kaynig, V.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods9(7), 676–682 (2012).
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E. J. Lee, T.-W. Kim, R. N. Weinreb, K. H. Park, S. H. Kim, and D. M. Kim, “Visualization of the lamina cribrosa using enhanced depth imaging spectral-domain optical coherence tomography,” Am. J. Ophthalmology152(1), 87–95 (2011).

Kim, S. H.

E. J. Lee, T.-W. Kim, R. N. Weinreb, K. H. Park, S. H. Kim, and D. M. Kim, “Visualization of the lamina cribrosa using enhanced depth imaging spectral-domain optical coherence tomography,” Am. J. Ophthalmology152(1), 87–95 (2011).

Kim, T.-W.

E. J. Lee, T.-W. Kim, R. N. Weinreb, K. H. Park, S. H. Kim, and D. M. Kim, “Visualization of the lamina cribrosa using enhanced depth imaging spectral-domain optical coherence tomography,” Am. J. Ophthalmology152(1), 87–95 (2011).

Kiumehr, S.

S. Kiumehr, S. C. Park, D. Syril, C. C. Teng, C. Tello, J. M. Liebmann, and R. Ritch, “In vivo evaluation of focal lamina cribrosa defects in glaucoma,” Arch. Ophthalmol.130(5), 552–559 (2012).
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M. Doube, M. M. Kłosowski, I. Arganda-Carreras, F. P. Cordelières, R. P. Dougherty, J. S. Jackson, B. Schmid, J. R. Hutchinson, and S. J. Shefelbine, “BoneJ: Free and extensible bone image analysis in ImageJ,” Bone47(6), 1076–1079 (2010).
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Kraus, M.

B. Wang, J. E. Nevins, Z. Nadler, G. Wollstein, H. Ishikawa, R. A. Bilonick, L. Kagemann, I. A. Sigal, I. Grulkowski, J. J. Liu, M. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “In vivo lamina cribrosa micro-architecture in healthy and glaucomatous eyes as assessed by optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.54(13), 8270–8274 (2013).
[CrossRef] [PubMed]

Kraus, M. F.

Lai, G. W. K.

C. K. S. Leung, S. Lam, R. N. Weinreb, S. Liu, C. Ye, L. Liu, J. He, G. W. K. Lai, T. Li, and D. S. Lam, “Retinal nerve fiber layer imaging with spectral-domain optical coherence tomography: analysis of the retinal nerve fiber layer map for glaucoma detection,” Ophthalmology117(9), 1684–1691 (2010).
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Lam, D. S.

C. K. S. Leung, S. Lam, R. N. Weinreb, S. Liu, C. Ye, L. Liu, J. He, G. W. K. Lai, T. Li, and D. S. Lam, “Retinal nerve fiber layer imaging with spectral-domain optical coherence tomography: analysis of the retinal nerve fiber layer map for glaucoma detection,” Ophthalmology117(9), 1684–1691 (2010).
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Lam, S.

C. K. S. Leung, S. Lam, R. N. Weinreb, S. Liu, C. Ye, L. Liu, J. He, G. W. K. Lai, T. Li, and D. S. Lam, “Retinal nerve fiber layer imaging with spectral-domain optical coherence tomography: analysis of the retinal nerve fiber layer map for glaucoma detection,” Ophthalmology117(9), 1684–1691 (2010).
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C. K. S. Leung, S. Lam, R. N. Weinreb, S. Liu, C. Ye, L. Liu, J. He, G. W. K. Lai, T. Li, and D. S. Lam, “Retinal nerve fiber layer imaging with spectral-domain optical coherence tomography: analysis of the retinal nerve fiber layer map for glaucoma detection,” Ophthalmology117(9), 1684–1691 (2010).
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K. M. Ivers, C. Li, N. Patel, N. Sredar, X. Luo, H. Queener, R. S. Harwerth, and J. Porter, “Reproducibility of measuring lamina cribrosa pore geometry in human and nonhuman primates with in vivo adaptive optics imaging,” Invest. Ophthalmol. Vis. Sci.52(8), 5473–5480 (2011).
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B. Wang, J. E. Nevins, Z. Nadler, G. Wollstein, H. Ishikawa, R. A. Bilonick, L. Kagemann, I. A. Sigal, I. Grulkowski, J. J. Liu, M. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “In vivo lamina cribrosa micro-architecture in healthy and glaucomatous eyes as assessed by optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.54(13), 8270–8274 (2013).
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O. Tan, V. Chopra, A. T.-H. Lu, J. S. Schuman, H. Ishikawa, G. Wollstein, R. Varma, and D. Huang, “Detection of macular ganglion cell loss in glaucoma by Fourier-domain optical coherence tomography,” Ophthalmology116(12), 2305 (2009).

O. Tan, G. Li, A. T.-H. Lu, R. Varma, D. Huang, and Advanced Imaging for Glaucoma Study Group, “Mapping of macular substructures with optical coherence tomography for glaucoma diagnosis,” Ophthalmology115(6), 949–956 (2008).
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Z. Nadler, B. Wang, G. Wollstein, J. E. Nevins, H. Ishikawa, L. Kagemann, I. A. Sigal, R. D. Ferguson, D. X. Hammer, I. Grulkowski, J. J. Liu, M. F. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “Automated lamina cribrosa microstructural segmentation in optical coherence tomography scans of healthy and glaucomatous eyes,” Biomed. Opt. Express4(11), 2596–2608 (2013).

B. Wang, J. E. Nevins, Z. Nadler, G. Wollstein, H. Ishikawa, R. A. Bilonick, L. Kagemann, I. A. Sigal, I. Grulkowski, J. J. Liu, M. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “In vivo lamina cribrosa micro-architecture in healthy and glaucomatous eyes as assessed by optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.54(13), 8270–8274 (2013).
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K. M. Ivers, C. Li, N. Patel, N. Sredar, X. Luo, H. Queener, R. S. Harwerth, and J. Porter, “Reproducibility of measuring lamina cribrosa pore geometry in human and nonhuman primates with in vivo adaptive optics imaging,” Invest. Ophthalmol. Vis. Sci.52(8), 5473–5480 (2011).
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Z. Nadler, B. Wang, G. Wollstein, J. E. Nevins, H. Ishikawa, L. Kagemann, I. A. Sigal, R. D. Ferguson, D. X. Hammer, I. Grulkowski, J. J. Liu, M. F. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “Automated lamina cribrosa microstructural segmentation in optical coherence tomography scans of healthy and glaucomatous eyes,” Biomed. Opt. Express4(11), 2596–2608 (2013).

B. Wang, J. E. Nevins, Z. Nadler, G. Wollstein, H. Ishikawa, R. A. Bilonick, L. Kagemann, I. A. Sigal, I. Grulkowski, J. J. Liu, M. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “In vivo lamina cribrosa micro-architecture in healthy and glaucomatous eyes as assessed by optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.54(13), 8270–8274 (2013).
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S. Kiumehr, S. C. Park, D. Syril, C. C. Teng, C. Tello, J. M. Liebmann, and R. Ritch, “In vivo evaluation of focal lamina cribrosa defects in glaucoma,” Arch. Ophthalmol.130(5), 552–559 (2012).
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S. Kiumehr, S. C. Park, D. Syril, C. C. Teng, C. Tello, J. M. Liebmann, and R. Ritch, “In vivo evaluation of focal lamina cribrosa defects in glaucoma,” Arch. Ophthalmol.130(5), 552–559 (2012).
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Rueden, C.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods9(7), 676–682 (2012).
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J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods9(7), 676–682 (2012).
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J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods9(7), 676–682 (2012).
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M. Doube, M. M. Kłosowski, I. Arganda-Carreras, F. P. Cordelières, R. P. Dougherty, J. S. Jackson, B. Schmid, J. R. Hutchinson, and S. J. Shefelbine, “BoneJ: Free and extensible bone image analysis in ImageJ,” Bone47(6), 1076–1079 (2010).
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R. Rezakhaniha, A. Agianniotis, J. T. C. Schrauwen, A. Griffa, D. Sage, C. V. C. Bouten, F. N. van de Vosse, M. Unser, and N. Stergiopulos, “Experimental investigation of collagen waviness and orientation in the arterial adventitia using confocal laser scanning microscopy,” Biomech. Model. Mechanobiol.11(3-4), 461–473 (2012).
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B. Wang, J. E. Nevins, Z. Nadler, G. Wollstein, H. Ishikawa, R. A. Bilonick, L. Kagemann, I. A. Sigal, I. Grulkowski, J. J. Liu, M. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “In vivo lamina cribrosa micro-architecture in healthy and glaucomatous eyes as assessed by optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.54(13), 8270–8274 (2013).
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O. Tan, V. Chopra, A. T.-H. Lu, J. S. Schuman, H. Ishikawa, G. Wollstein, R. Varma, and D. Huang, “Detection of macular ganglion cell loss in glaucoma by Fourier-domain optical coherence tomography,” Ophthalmology116(12), 2305 (2009).

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M. Doube, M. M. Kłosowski, I. Arganda-Carreras, F. P. Cordelières, R. P. Dougherty, J. S. Jackson, B. Schmid, J. R. Hutchinson, and S. J. Shefelbine, “BoneJ: Free and extensible bone image analysis in ImageJ,” Bone47(6), 1076–1079 (2010).
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B. Wang, J. E. Nevins, Z. Nadler, G. Wollstein, H. Ishikawa, R. A. Bilonick, L. Kagemann, I. A. Sigal, I. Grulkowski, J. J. Liu, M. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “In vivo lamina cribrosa micro-architecture in healthy and glaucomatous eyes as assessed by optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.54(13), 8270–8274 (2013).
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Sredar, N.

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[CrossRef] [PubMed]

K. M. Ivers, C. Li, N. Patel, N. Sredar, X. Luo, H. Queener, R. S. Harwerth, and J. Porter, “Reproducibility of measuring lamina cribrosa pore geometry in human and nonhuman primates with in vivo adaptive optics imaging,” Invest. Ophthalmol. Vis. Sci.52(8), 5473–5480 (2011).
[CrossRef] [PubMed]

Stergiopulos, N.

R. Rezakhaniha, A. Agianniotis, J. T. C. Schrauwen, A. Griffa, D. Sage, C. V. C. Bouten, F. N. van de Vosse, M. Unser, and N. Stergiopulos, “Experimental investigation of collagen waviness and orientation in the arterial adventitia using confocal laser scanning microscopy,” Biomech. Model. Mechanobiol.11(3-4), 461–473 (2012).
[CrossRef] [PubMed]

Strouthidis, N. G.

N. G. Strouthidis, S. Demirel, R. Asaoka, C. Cossio-Zuniga, and D. F. Garway-Heath, “The Heidelberg retina tomograph Glaucoma Probability Score: reproducibility and measurement of progression,” Ophthalmology117(4), 724–729 (2010).
[CrossRef] [PubMed]

Suen, C. Y.

T. Y. Zhang and C. Y. Suen, “A fast parallel algorithm for thinning digital patterns,” Commun. ACM27(3), 236–239 (1984).

Susanna, R.

F. A. Medeiros, L. M. Zangwill, C. Bowd, R. M. Vessani, R. Susanna, and R. N. Weinreb, “Evaluation of retinal nerve fiber layer, optic nerve head, and macular thickness measurements for glaucoma detection using optical coherence tomography,” Am. J. Ophthalmol.139(1), 44–55 (2005).
[CrossRef] [PubMed]

Syril, D.

S. Kiumehr, S. C. Park, D. Syril, C. C. Teng, C. Tello, J. M. Liebmann, and R. Ritch, “In vivo evaluation of focal lamina cribrosa defects in glaucoma,” Arch. Ophthalmol.130(5), 552–559 (2012).
[PubMed]

Takayama, K.

T. Akagi, M. Hangai, K. Takayama, A. Nonaka, S. Ooto, and N. Yoshimura, “In vivo imaging of lamina cribrosa pores by adaptive optics scanning laser ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci.53(7), 4111–4119 (2012).
[CrossRef] [PubMed]

Tan, O.

O. Tan, V. Chopra, A. T.-H. Lu, J. S. Schuman, H. Ishikawa, G. Wollstein, R. Varma, and D. Huang, “Detection of macular ganglion cell loss in glaucoma by Fourier-domain optical coherence tomography,” Ophthalmology116(12), 2305 (2009).

O. Tan, G. Li, A. T.-H. Lu, R. Varma, D. Huang, and Advanced Imaging for Glaucoma Study Group, “Mapping of macular substructures with optical coherence tomography for glaucoma diagnosis,” Ophthalmology115(6), 949–956 (2008).
[CrossRef] [PubMed]

Tatham, A. J.

A. J. Tatham, A. Miki, R. N. Weinreb, L. M. Zangwill, and F. A. Medeiros, “Defects of the lamina cribrosa in eyes with localized retinal nerve fiber layer loss,” Ophthalmology121, 110–118 (2014).
[PubMed]

Tello, C.

S. Kiumehr, S. C. Park, D. Syril, C. C. Teng, C. Tello, J. M. Liebmann, and R. Ritch, “In vivo evaluation of focal lamina cribrosa defects in glaucoma,” Arch. Ophthalmol.130(5), 552–559 (2012).
[PubMed]

Teng, C. C.

S. Kiumehr, S. C. Park, D. Syril, C. C. Teng, C. Tello, J. M. Liebmann, and R. Ritch, “In vivo evaluation of focal lamina cribrosa defects in glaucoma,” Arch. Ophthalmol.130(5), 552–559 (2012).
[PubMed]

Tertinegg, I.

I. A. Sigal, J. G. Flanagan, I. Tertinegg, and C. R. Ethier, “3D morphometry of the human optic nerve head,” Exp. Eye Res.90(1), 70–80 (2010).
[CrossRef] [PubMed]

Tezel, G.

G. Tezel, K. Trinkaus, and M. B. Wax, “Alterations in the morphology of lamina cribrosa pores in glaucomatous eyes,” Br. J. Ophthalmol.88(2), 251–256 (2004).
[CrossRef] [PubMed]

Tinevez, J. Y.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods9(7), 676–682 (2012).
[CrossRef] [PubMed]

Tomancak, P.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods9(7), 676–682 (2012).
[CrossRef] [PubMed]

Torti, C.

Townsend, K. A.

K. A. Townsend, G. Wollstein, and J. S. Schuman, “Imaging of the retinal nerve fibre layer for glaucoma,” Br. J. Ophthalmol.93(2), 139–143 (2009).
[CrossRef] [PubMed]

Trinkaus, K.

G. Tezel, K. Trinkaus, and M. B. Wax, “Alterations in the morphology of lamina cribrosa pores in glaucomatous eyes,” Br. J. Ophthalmol.88(2), 251–256 (2004).
[CrossRef] [PubMed]

Unser, M.

R. Rezakhaniha, A. Agianniotis, J. T. C. Schrauwen, A. Griffa, D. Sage, C. V. C. Bouten, F. N. van de Vosse, M. Unser, and N. Stergiopulos, “Experimental investigation of collagen waviness and orientation in the arterial adventitia using confocal laser scanning microscopy,” Biomech. Model. Mechanobiol.11(3-4), 461–473 (2012).
[CrossRef] [PubMed]

Unterhuber, A.

van de Vosse, F. N.

R. Rezakhaniha, A. Agianniotis, J. T. C. Schrauwen, A. Griffa, D. Sage, C. V. C. Bouten, F. N. van de Vosse, M. Unser, and N. Stergiopulos, “Experimental investigation of collagen waviness and orientation in the arterial adventitia using confocal laser scanning microscopy,” Biomech. Model. Mechanobiol.11(3-4), 461–473 (2012).
[CrossRef] [PubMed]

Varma, R.

O. Tan, V. Chopra, A. T.-H. Lu, J. S. Schuman, H. Ishikawa, G. Wollstein, R. Varma, and D. Huang, “Detection of macular ganglion cell loss in glaucoma by Fourier-domain optical coherence tomography,” Ophthalmology116(12), 2305 (2009).

O. Tan, G. Li, A. T.-H. Lu, R. Varma, D. Huang, and Advanced Imaging for Glaucoma Study Group, “Mapping of macular substructures with optical coherence tomography for glaucoma diagnosis,” Ophthalmology115(6), 949–956 (2008).
[CrossRef] [PubMed]

Vessani, R. M.

F. A. Medeiros, L. M. Zangwill, C. Bowd, R. M. Vessani, R. Susanna, and R. N. Weinreb, “Evaluation of retinal nerve fiber layer, optic nerve head, and macular thickness measurements for glaucoma detection using optical coherence tomography,” Am. J. Ophthalmol.139(1), 44–55 (2005).
[CrossRef] [PubMed]

Vilupuru, A. S.

Voinea, L.

C. Alexandrescu, A. M. Dascalu, A. Panca, A. Sescioreanu, C. Mitulescu, R. Ciuluvica, L. Voinea, and C. Celea, “Confocal scanning laser ophthalmoscopy in glaucoma diagnosis and management,” J. Med. Life3(3), 229–234 (2010).
[PubMed]

Wang, B.

Z. Nadler, B. Wang, G. Wollstein, J. E. Nevins, H. Ishikawa, L. Kagemann, I. A. Sigal, R. D. Ferguson, D. X. Hammer, I. Grulkowski, J. J. Liu, M. F. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “Automated lamina cribrosa microstructural segmentation in optical coherence tomography scans of healthy and glaucomatous eyes,” Biomed. Opt. Express4(11), 2596–2608 (2013).

B. Wang, J. E. Nevins, Z. Nadler, G. Wollstein, H. Ishikawa, R. A. Bilonick, L. Kagemann, I. A. Sigal, I. Grulkowski, J. J. Liu, M. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “In vivo lamina cribrosa micro-architecture in healthy and glaucomatous eyes as assessed by optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.54(13), 8270–8274 (2013).
[CrossRef] [PubMed]

Wang, J.

G. Wollstein, H. Ishikawa, J. Wang, S. A. Beaton, and J. S. Schuman, “Comparison of three optical coherence tomography scanning areas for detection of glaucomatous damage,” Am. J. Ophthalmol.139(1), 39–43 (2005).
[CrossRef] [PubMed]

Wax, M. B.

G. Tezel, K. Trinkaus, and M. B. Wax, “Alterations in the morphology of lamina cribrosa pores in glaucomatous eyes,” Br. J. Ophthalmol.88(2), 251–256 (2004).
[CrossRef] [PubMed]

Weinreb, R. N.

A. J. Tatham, A. Miki, R. N. Weinreb, L. M. Zangwill, and F. A. Medeiros, “Defects of the lamina cribrosa in eyes with localized retinal nerve fiber layer loss,” Ophthalmology121, 110–118 (2014).
[PubMed]

E. J. Lee, T.-W. Kim, R. N. Weinreb, K. H. Park, S. H. Kim, and D. M. Kim, “Visualization of the lamina cribrosa using enhanced depth imaging spectral-domain optical coherence tomography,” Am. J. Ophthalmology152(1), 87–95 (2011).

C. K. S. Leung, S. Lam, R. N. Weinreb, S. Liu, C. Ye, L. Liu, J. He, G. W. K. Lai, T. Li, and D. S. Lam, “Retinal nerve fiber layer imaging with spectral-domain optical coherence tomography: analysis of the retinal nerve fiber layer map for glaucoma detection,” Ophthalmology117(9), 1684–1691 (2010).
[CrossRef] [PubMed]

D. Ng, L. M. Zangwill, L. Racette, C. Bowd, J. P. Pascual, R. R. A. Bourne, C. Boden, R. N. Weinreb, and P. A. Sample, “Agreement and repeatability for standard automated perimetry and confocal scanning laser ophthalmoscopy in the diagnostic innovations in glaucoma study,” Am. J. Ophthalmol.142(3), 381–386 (2006).
[CrossRef] [PubMed]

F. A. Medeiros, L. M. Zangwill, C. Bowd, R. M. Vessani, R. Susanna, and R. N. Weinreb, “Evaluation of retinal nerve fiber layer, optic nerve head, and macular thickness measurements for glaucoma detection using optical coherence tomography,” Am. J. Ophthalmol.139(1), 44–55 (2005).
[CrossRef] [PubMed]

Werner, J. S.

White, D. J.

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods9(7), 676–682 (2012).
[CrossRef] [PubMed]

Winkler, M.

M. Winkler, B. Jester, C. Nien-Shy, S. Massei, D. S. Minckler, J. V. Jester, and D. J. Brown, “High resolution three-dimensional reconstruction of the collagenous matrix of the human optic nerve head,” Brain Res. Bull.81(2-3), 339–348 (2010).
[CrossRef] [PubMed]

Wollstein, G.

Z. Nadler, B. Wang, G. Wollstein, J. E. Nevins, H. Ishikawa, L. Kagemann, I. A. Sigal, R. D. Ferguson, D. X. Hammer, I. Grulkowski, J. J. Liu, M. F. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “Automated lamina cribrosa microstructural segmentation in optical coherence tomography scans of healthy and glaucomatous eyes,” Biomed. Opt. Express4(11), 2596–2608 (2013).

B. Wang, J. E. Nevins, Z. Nadler, G. Wollstein, H. Ishikawa, R. A. Bilonick, L. Kagemann, I. A. Sigal, I. Grulkowski, J. J. Liu, M. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “In vivo lamina cribrosa micro-architecture in healthy and glaucomatous eyes as assessed by optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.54(13), 8270–8274 (2013).
[CrossRef] [PubMed]

O. Tan, V. Chopra, A. T.-H. Lu, J. S. Schuman, H. Ishikawa, G. Wollstein, R. Varma, and D. Huang, “Detection of macular ganglion cell loss in glaucoma by Fourier-domain optical coherence tomography,” Ophthalmology116(12), 2305 (2009).

K. A. Townsend, G. Wollstein, and J. S. Schuman, “Imaging of the retinal nerve fibre layer for glaucoma,” Br. J. Ophthalmol.93(2), 139–143 (2009).
[CrossRef] [PubMed]

G. Wollstein, H. Ishikawa, J. Wang, S. A. Beaton, and J. S. Schuman, “Comparison of three optical coherence tomography scanning areas for detection of glaucomatous damage,” Am. J. Ophthalmol.139(1), 39–43 (2005).
[CrossRef] [PubMed]

Ye, C.

C. K. S. Leung, S. Lam, R. N. Weinreb, S. Liu, C. Ye, L. Liu, J. He, G. W. K. Lai, T. Li, and D. S. Lam, “Retinal nerve fiber layer imaging with spectral-domain optical coherence tomography: analysis of the retinal nerve fiber layer map for glaucoma detection,” Ophthalmology117(9), 1684–1691 (2010).
[CrossRef] [PubMed]

Yoshimura, N.

T. Akagi, M. Hangai, K. Takayama, A. Nonaka, S. Ooto, and N. Yoshimura, “In vivo imaging of lamina cribrosa pores by adaptive optics scanning laser ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci.53(7), 4111–4119 (2012).
[CrossRef] [PubMed]

Zangwill, L. M.

A. J. Tatham, A. Miki, R. N. Weinreb, L. M. Zangwill, and F. A. Medeiros, “Defects of the lamina cribrosa in eyes with localized retinal nerve fiber layer loss,” Ophthalmology121, 110–118 (2014).
[PubMed]

D. Ng, L. M. Zangwill, L. Racette, C. Bowd, J. P. Pascual, R. R. A. Bourne, C. Boden, R. N. Weinreb, and P. A. Sample, “Agreement and repeatability for standard automated perimetry and confocal scanning laser ophthalmoscopy in the diagnostic innovations in glaucoma study,” Am. J. Ophthalmol.142(3), 381–386 (2006).
[CrossRef] [PubMed]

F. A. Medeiros, L. M. Zangwill, C. Bowd, R. M. Vessani, R. Susanna, and R. N. Weinreb, “Evaluation of retinal nerve fiber layer, optic nerve head, and macular thickness measurements for glaucoma detection using optical coherence tomography,” Am. J. Ophthalmol.139(1), 44–55 (2005).
[CrossRef] [PubMed]

Zawadzki, R. J.

Zhang, T. Y.

T. Y. Zhang and C. Y. Suen, “A fast parallel algorithm for thinning digital patterns,” Commun. ACM27(3), 236–239 (1984).

Zouridakis, G.

Am. J. Ophthalmol. (3)

G. Wollstein, H. Ishikawa, J. Wang, S. A. Beaton, and J. S. Schuman, “Comparison of three optical coherence tomography scanning areas for detection of glaucomatous damage,” Am. J. Ophthalmol.139(1), 39–43 (2005).
[CrossRef] [PubMed]

F. A. Medeiros, L. M. Zangwill, C. Bowd, R. M. Vessani, R. Susanna, and R. N. Weinreb, “Evaluation of retinal nerve fiber layer, optic nerve head, and macular thickness measurements for glaucoma detection using optical coherence tomography,” Am. J. Ophthalmol.139(1), 44–55 (2005).
[CrossRef] [PubMed]

D. Ng, L. M. Zangwill, L. Racette, C. Bowd, J. P. Pascual, R. R. A. Bourne, C. Boden, R. N. Weinreb, and P. A. Sample, “Agreement and repeatability for standard automated perimetry and confocal scanning laser ophthalmoscopy in the diagnostic innovations in glaucoma study,” Am. J. Ophthalmol.142(3), 381–386 (2006).
[CrossRef] [PubMed]

Am. J. Ophthalmology (1)

E. J. Lee, T.-W. Kim, R. N. Weinreb, K. H. Park, S. H. Kim, and D. M. Kim, “Visualization of the lamina cribrosa using enhanced depth imaging spectral-domain optical coherence tomography,” Am. J. Ophthalmology152(1), 87–95 (2011).

Arch. Ophthalmol. (3)

S. Kiumehr, S. C. Park, D. Syril, C. C. Teng, C. Tello, J. M. Liebmann, and R. Ritch, “In vivo evaluation of focal lamina cribrosa defects in glaucoma,” Arch. Ophthalmol.130(5), 552–559 (2012).
[PubMed]

H. A. Quigley and E. M. Addicks, “Regional differences in the structure of the lamina cribrosa and their relation to glaucomatous optic nerve damage,” Arch. Ophthalmol.99(1), 137–143 (1981).
[CrossRef] [PubMed]

L. Dandona, H. A. Quigley, A. E. Brown, and C. Enger, “Quantitative regional structure of the normal human lamina cribrosa. A racial comparison,” Arch. Ophthalmol.108(3), 393–398 (1990).
[CrossRef] [PubMed]

Biomech. Model. Mechanobiol. (2)

R. Rezakhaniha, A. Agianniotis, J. T. C. Schrauwen, A. Griffa, D. Sage, C. V. C. Bouten, F. N. van de Vosse, M. Unser, and N. Stergiopulos, “Experimental investigation of collagen waviness and orientation in the arterial adventitia using confocal laser scanning microscopy,” Biomech. Model. Mechanobiol.11(3-4), 461–473 (2012).
[CrossRef] [PubMed]

R. Grytz, G. Meschke, and J. B. Jonas, “The collagen fibril architecture in the lamina cribrosa and peripapillary sclera predicted by a computational remodeling approach,” Biomech. Model. Mechanobiol.10(3), 371–382 (2011).
[CrossRef] [PubMed]

Biomed. Opt. Express (2)

Bone (1)

M. Doube, M. M. Kłosowski, I. Arganda-Carreras, F. P. Cordelières, R. P. Dougherty, J. S. Jackson, B. Schmid, J. R. Hutchinson, and S. J. Shefelbine, “BoneJ: Free and extensible bone image analysis in ImageJ,” Bone47(6), 1076–1079 (2010).
[CrossRef] [PubMed]

Br. J. Ophthalmol. (3)

G. Tezel, K. Trinkaus, and M. B. Wax, “Alterations in the morphology of lamina cribrosa pores in glaucomatous eyes,” Br. J. Ophthalmol.88(2), 251–256 (2004).
[CrossRef] [PubMed]

H. A. Quigley and A. T. Broman, “The number of people with glaucoma worldwide in 2010 and 2020,” Br. J. Ophthalmol.90(3), 262–267 (2006).
[CrossRef] [PubMed]

K. A. Townsend, G. Wollstein, and J. S. Schuman, “Imaging of the retinal nerve fibre layer for glaucoma,” Br. J. Ophthalmol.93(2), 139–143 (2009).
[CrossRef] [PubMed]

Brain Res. Bull. (1)

M. Winkler, B. Jester, C. Nien-Shy, S. Massei, D. S. Minckler, J. V. Jester, and D. J. Brown, “High resolution three-dimensional reconstruction of the collagenous matrix of the human optic nerve head,” Brain Res. Bull.81(2-3), 339–348 (2010).
[CrossRef] [PubMed]

Commun. ACM (1)

T. Y. Zhang and C. Y. Suen, “A fast parallel algorithm for thinning digital patterns,” Commun. ACM27(3), 236–239 (1984).

Curr. Eye Res. (1)

L. Fontana, A. Bhandari, F. W. Fitzke, and R. A. Hitchings, “In vivo morphometry of the lamina cribrosa and its relation to visual field loss in glaucoma,” Curr. Eye Res.17(4), 363–369 (1998).
[CrossRef] [PubMed]

Exp. Eye Res. (1)

I. A. Sigal, J. G. Flanagan, I. Tertinegg, and C. R. Ethier, “3D morphometry of the human optic nerve head,” Exp. Eye Res.90(1), 70–80 (2010).
[CrossRef] [PubMed]

Invest. Ophthalmol. Vis. Sci. (5)

B. Wang, J. E. Nevins, Z. Nadler, G. Wollstein, H. Ishikawa, R. A. Bilonick, L. Kagemann, I. A. Sigal, I. Grulkowski, J. J. Liu, M. Kraus, C. D. Lu, J. Hornegger, J. G. Fujimoto, and J. S. Schuman, “In vivo lamina cribrosa micro-architecture in healthy and glaucomatous eyes as assessed by optical coherence tomography,” Invest. Ophthalmol. Vis. Sci.54(13), 8270–8274 (2013).
[CrossRef] [PubMed]

T. Akagi, M. Hangai, K. Takayama, A. Nonaka, S. Ooto, and N. Yoshimura, “In vivo imaging of lamina cribrosa pores by adaptive optics scanning laser ophthalmoscopy,” Invest. Ophthalmol. Vis. Sci.53(7), 4111–4119 (2012).
[CrossRef] [PubMed]

K. M. Ivers, C. Li, N. Patel, N. Sredar, X. Luo, H. Queener, R. S. Harwerth, and J. Porter, “Reproducibility of measuring lamina cribrosa pore geometry in human and nonhuman primates with in vivo adaptive optics imaging,” Invest. Ophthalmol. Vis. Sci.52(8), 5473–5480 (2011).
[CrossRef] [PubMed]

H. A. Quigley, “Glaucoma: macrocosm to microcosm the Friedenwald lecture,” Invest. Ophthalmol. Vis. Sci.46(8), 2663–2670 (2005).
[CrossRef] [PubMed]

M. D. Roberts, V. Grau, J. Grimm, J. Reynaud, A. J. Bellezza, C. F. Burgoyne, and J. C. Downs, “Remodeling of the connective tissue microarchitecture of the lamina cribrosa in early experimental glaucoma,” Invest. Ophthalmol. Vis. Sci.50(2), 681–690 (2008).
[CrossRef] [PubMed]

J. Med. Life (1)

C. Alexandrescu, A. M. Dascalu, A. Panca, A. Sescioreanu, C. Mitulescu, R. Ciuluvica, L. Voinea, and C. Celea, “Confocal scanning laser ophthalmoscopy in glaucoma diagnosis and management,” J. Med. Life3(3), 229–234 (2010).
[PubMed]

J. Opt. Soc. Am. A (2)

Lancet (1)

J. M. Bland and D. G. Altman, “Statistical methods for assessing agreement between two methods of clinical measurement,” Lancet327(8476), 307–310 (1986).
[CrossRef] [PubMed]

Nat. Methods (1)

J. Schindelin, I. Arganda-Carreras, E. Frise, V. Kaynig, M. Longair, T. Pietzsch, S. Preibisch, C. Rueden, S. Saalfeld, B. Schmid, J. Y. Tinevez, D. J. White, V. Hartenstein, K. Eliceiri, P. Tomancak, and A. Cardona, “Fiji: an open-source platform for biological-image analysis,” Nat. Methods9(7), 676–682 (2012).
[CrossRef] [PubMed]

Ophthalmology (6)

N. G. Strouthidis, S. Demirel, R. Asaoka, C. Cossio-Zuniga, and D. F. Garway-Heath, “The Heidelberg retina tomograph Glaucoma Probability Score: reproducibility and measurement of progression,” Ophthalmology117(4), 724–729 (2010).
[CrossRef] [PubMed]

A. J. Tatham, A. Miki, R. N. Weinreb, L. M. Zangwill, and F. A. Medeiros, “Defects of the lamina cribrosa in eyes with localized retinal nerve fiber layer loss,” Ophthalmology121, 110–118 (2014).
[PubMed]

H.-Y. L. Park, S. H. Jeon, and C. K. Park, “Enhanced depth imaging detects lamina cribrosa thickness differences in normal tension glaucoma and primary open-angle glaucoma,” Ophthalmology119(1), 10–20 (2012).
[CrossRef] [PubMed]

C. K. S. Leung, S. Lam, R. N. Weinreb, S. Liu, C. Ye, L. Liu, J. He, G. W. K. Lai, T. Li, and D. S. Lam, “Retinal nerve fiber layer imaging with spectral-domain optical coherence tomography: analysis of the retinal nerve fiber layer map for glaucoma detection,” Ophthalmology117(9), 1684–1691 (2010).
[CrossRef] [PubMed]

O. Tan, G. Li, A. T.-H. Lu, R. Varma, D. Huang, and Advanced Imaging for Glaucoma Study Group, “Mapping of macular substructures with optical coherence tomography for glaucoma diagnosis,” Ophthalmology115(6), 949–956 (2008).
[CrossRef] [PubMed]

O. Tan, V. Chopra, A. T.-H. Lu, J. S. Schuman, H. Ishikawa, G. Wollstein, R. Varma, and D. Huang, “Detection of macular ganglion cell loss in glaucoma by Fourier-domain optical coherence tomography,” Ophthalmology116(12), 2305 (2009).

Opt. Express (2)

Ultrasound Obstet. Gynecol. (1)

J. W. Bartlett and C. Frost, “Reliability, repeatability and reproducibility: analysis of measurement errors in continuous variables,” Ultrasound Obstet. Gynecol.31(4), 466–475 (2008).
[CrossRef] [PubMed]

Other (1)

J. L. Jaech, Statistical Analysis of Measurement Errors (Exxon Monographs Series), 1 ed. (Wiley 1985).

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Figures (6)

Fig. 1
Fig. 1

6° scan of the lamina cribrosa taken as the confocal scanning laser ophthalmoscopy (CSLO) frame pans horizontally across the volume. AO-SDOCT (right of each pane) shows the tissue cross-section corresponding to the center of the CSLO frame, which is then used to register and reconstruct the volume.

Fig. 2
Fig. 2

3D LC (a) and C-scan (b,e) visualization (a) is segmented in C-mode slices (c,f) permitting the quantification of structural parameters such as beam thickness where thicker beams are shown in yellow and thinner beams are purple (d,g).

Fig. 3
Fig. 3

Repeated C-mode slices of the same eye with pore segmentation (a, b) and skeleton presentation of the beams (d, e). Segmentation is overlaid on C-mode from similar location and compared with yellow color representing full agreement (c, f).

Fig. 4
Fig. 4

Pore volumes for repeat scans visualized in 3D (left) and histogram of cross-sectional pore area (right) sampled in C-mode slices shows qualitative agreement between scans. Differences in visualizable lamina manifest as differences in pore count for excluded pores.

Fig. 5
Fig. 5

C-mode slices taken from repeated scans of a glaucomatous eye are colored by beam orientation (left) which translates to a similar distribution shape for beam orientation angle between scans (right). Orientation analysis includes all C-mode slices in the LC.

Fig. 6
Fig. 6

Bland-Altman plots of pore diameter separated by distribution percentile. Lines show the 95% confidence intervals for paired differences. Measurement spread is fairly consistent through all pore sizes.

Tables (1)

Tables Icon

Table 1 Mean parameter values for segmentations of LC and their imprecision

Metrics