Abstract

Microcystic macular edema (MME) manifests as small, hyporeflective cystic areas within the retina. For reasons that are still largely unknown, a small proportion of patients with multiple sclerosis (MS) develop MME—predominantly in the inner nuclear layer. These cystoid spaces, denoted pseudocysts, can be imaged using optical coherence tomography (OCT) where they appear as small, discrete, low intensity areas with high contrast to the surrounding tissue. The ability to automatically segment these pseudocysts would enable a more detailed study of MME than has been previously possible. Although larger pseudocysts often appear quite clearly in the OCT images, the multi-frame averaging performed by the Spectralis scanner adds a significant amount of variability to the appearance of smaller pseudocysts. Thus, simple segmentation methods only incorporating intensity information do not perform well. In this work, we propose to use a random forest classifier to classify the MME pixels. An assortment of both intensity and spatial features are used to aid the classification. Using a cross-validation evaluation strategy with manual delineation as ground truth, our method is able to correctly identify 79% of pseudocysts with a precision of 85%. Finally, we constructed a classifier from the output of our algorithm to distinguish clinically identified MME from non-MME subjects yielding an accuracy of 92%.

© 2014 Optical Society of America

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References

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  1. A. J. Green, S. McQuaid, S. L. Hauser, I. V. Allen, and R. Lyness, “Ocular pathology in multiple sclerosis: retinal atrophy and inflammation irrespective of disease duration,” Brain 133, 1591–1601 (2010).
    [Crossref] [PubMed]
  2. A. Petzold, J. F. de Boer, S. Schippling, P. Vermersch, R. Kardon, A. Green, P. A. Calabresi, and C. Polman, “Optical coherence tomography in multiple sclerosis: a systematic review and meta-analysis,” Lancet Neurol. 9, 921–932 (2010).
    [Crossref] [PubMed]
  3. J. B. Fisher, D. A. Jacobs, C. E. Markowitz, S. L. Galetta, N. J. Volpe, M. L. Nano-Schiavi, M. L. Baier, E. M. Frohman, H. Winslow, T. C. Frohman, P. A. Calabresi, M. G. Maguire, G. R. Cutter, and L. J. Balcer, “Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis,” Ophthalmology 113, 324–332 (2006).
    [Crossref] [PubMed]
  4. J. N. Ratchford, S. Saidha, E. S. Sotirchos, J. A. Oh, M. A. Seigo, C. Eckstein, M. K. Durbin, J. D. Oakley, S. A. Meyer, A. Conger, T. C. Frohman, S. D. Newsome, L. J. Balcer, E. M. Frohman, and P. A. Calabresi, “Active MS is associated with accelerated retinal ganglion cell/inner plexiform layer thinning,” Neurology 80, 47–54 (2013).
    [Crossref]
  5. J. M. Gelfand, R. Nolan, D. M. Schwartz, J. Graves, and A. J. Green, “Microcystic macular oedema in multiple sclerosis is associated with disease severity,” Brain 135, 1786–1793 (2012).
    [Crossref] [PubMed]
  6. S. Saidha, E. S. Sotirchos, M. A. Ibrahim, C. M. Crainiceanu, J. M. Gelfand, Y. J. Sepah, J. N. Ratchford, J. Oh, M. A. Seigo, S. D. Newsome, L. J. Balcer, E. M. Frohman, A. J. Green, Q. D. Nguyen, and P. A. Calabresi, “Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study,” Lancet Neurol. 11, 963–972 (2012).
    [Crossref] [PubMed]
  7. P. Barboni, V. Carelli, and G. Savini, “Microcystic macular degeneration from optic neuropathy: not inflammatory, not trans-synaptic degeneration,” Brain 136, e239 (2013).
    [Crossref] [PubMed]
  8. M. C. Burggraaff, J. Trieu, W. A. E. J. de Vries-Knoppert, L. Balk, and A. Petzold, “The clinical spectrum of microcystic macular edema,” Invest. Ophthalmol. Vis. Sci. 55, 952–961 (2014).
    [Crossref] [PubMed]
  9. P. Bhargava and P. A. Calabresi, “The expanding spectrum of aetiologies causing retinal microcystic macular change,” Brain 136, 3212–3214 (2013).
    [Crossref] [PubMed]
  10. E. K. Swingle, A. Lang, A. Carass, P. A. Calabresi, H. S. Ying, and J. L. Prince, “Microcystic macular edema detection in retina OCT images,” Proc. SPIE 9038, 90380O (2014).
    [Crossref]
  11. D. Fernandez, “Delineating fluid-filled region boundaries in optical coherence tomography images of the retina,” IEEE Trans. Med. Imag. 24, 929–945 (2005).
    [Crossref]
  12. Y. Zheng, J. Sahni, C. Campa, A. N. Stangos, A. Raj, and S. P. Harding, “Computerized assessment of intraretinal and subretinal fluid regions in spectral-domain optical coherence tomography images of the retina,” Am. J. Ophthalmol. 155, 277–286 (2013).
    [Crossref]
  13. X. Chen, M. Niemeijer, L. Zhang, K. Lee, M. Abramoff, and M. Sonka, “Three-dimensional segmentation of fluid-associated abnormalities in retinal OCT: probability constrained graph-search-graph-cut,” IEEE Trans. Med. Imag. 31, 1521–1531 (2012).
    [Crossref]
  14. S. J. Chiu, C. A. Toth, C. B. Rickman, J. A. Izatt, and S. Farsiu, “Automatic segmentation of closed-contour features in ophthalmic images using graph theory and dynamic programming,” Biomed. Opt. Express 3, 1127–1140 (2012).
    [Crossref] [PubMed]
  15. G. Wilkins, O. Houghton, and A. Oldenburg, “Automated segmentation of intraretinal cystoid fluid in optical coherence tomography,” IEEE Trans. Biomed. Eng. 59, 1109–1114 (2012).
    [Crossref] [PubMed]
  16. M. Pilch, K. Stieger, Y. Wenner, M. N. Preising, C. Friedburg, E. Meyer zu Bexten, and B. Lorenz, “Automated segmentation of pathological cavities in optical coherence tomography scans,” Invest. Ophthalmol. Vis. Sci. 54, 4385–4393 (2013).
    [Crossref] [PubMed]
  17. A. Lang, A. Carass, M. Hauser, E. S. Sotirchos, P. A. Calabresi, H. S. Ying, and J. L. Prince, “Retinal layer segmentation of macular OCT images using boundary classification,” Biomed. Opt. Express 4, 1133–1152 (2013).
    [Crossref] [PubMed]
  18. B. J. Antony, M. D. Abràmoff, M. M. Harper, W. Jeong, E. H. Sohn, Y. H. Kwon, R. Kardon, and M. K. Garvin, “A combined machine-learning and graph-based framework for the segmentation of retinal surfaces in SD-OCT volumes,” Biomed. Opt. Express 4, 2712–2728 (2013).
    [Crossref]
  19. B. J. Antony, M. S. Miri, M. D. Abràmoff, Y. H. Kwon, and M. K. Garvin, “Automated 3D segmentation of multiple surfaces with a shared hole: segmentation of the neural canal opening in SD-OCT volumes,” in Proceedings of the International Conference on Medical Image Computing and Computer-Assisted Intervention, P. Golland, N. Hata, C. Barillot, J. Hornegger, and R. Howe, eds. (Springer, 2014), pp. 739–746.
  20. P. Dufour, S. De Zanet, U. Wolf-Schnurrbusch, and J. Kowal, “Classification of drusen positions in optical coherence tomography data from patients with age-related macular degeneration,” in Proceedings of the International Conference on Pattern Recognition, (IEEE, 2012), pp. 2067–2070.
  21. L. Breiman, “Random forests,” Machine Learning 45, 5–32 (2001).
    [Crossref]
  22. F. Kaufhold, H. Zimmermann, E. Schneider, K. Ruprecht, F. Paul, T. Oberwahrenbrock, and A. U. Brandt, “Optic neuritis is associated with inner nuclear layer thickening and microcystic macular edema independently of multiple sclerosis,” PLoS ONE 8, e71145 (2013).
    [Crossref] [PubMed]

2014 (2)

M. C. Burggraaff, J. Trieu, W. A. E. J. de Vries-Knoppert, L. Balk, and A. Petzold, “The clinical spectrum of microcystic macular edema,” Invest. Ophthalmol. Vis. Sci. 55, 952–961 (2014).
[Crossref] [PubMed]

E. K. Swingle, A. Lang, A. Carass, P. A. Calabresi, H. S. Ying, and J. L. Prince, “Microcystic macular edema detection in retina OCT images,” Proc. SPIE 9038, 90380O (2014).
[Crossref]

2013 (8)

P. Bhargava and P. A. Calabresi, “The expanding spectrum of aetiologies causing retinal microcystic macular change,” Brain 136, 3212–3214 (2013).
[Crossref] [PubMed]

J. N. Ratchford, S. Saidha, E. S. Sotirchos, J. A. Oh, M. A. Seigo, C. Eckstein, M. K. Durbin, J. D. Oakley, S. A. Meyer, A. Conger, T. C. Frohman, S. D. Newsome, L. J. Balcer, E. M. Frohman, and P. A. Calabresi, “Active MS is associated with accelerated retinal ganglion cell/inner plexiform layer thinning,” Neurology 80, 47–54 (2013).
[Crossref]

Y. Zheng, J. Sahni, C. Campa, A. N. Stangos, A. Raj, and S. P. Harding, “Computerized assessment of intraretinal and subretinal fluid regions in spectral-domain optical coherence tomography images of the retina,” Am. J. Ophthalmol. 155, 277–286 (2013).
[Crossref]

M. Pilch, K. Stieger, Y. Wenner, M. N. Preising, C. Friedburg, E. Meyer zu Bexten, and B. Lorenz, “Automated segmentation of pathological cavities in optical coherence tomography scans,” Invest. Ophthalmol. Vis. Sci. 54, 4385–4393 (2013).
[Crossref] [PubMed]

A. Lang, A. Carass, M. Hauser, E. S. Sotirchos, P. A. Calabresi, H. S. Ying, and J. L. Prince, “Retinal layer segmentation of macular OCT images using boundary classification,” Biomed. Opt. Express 4, 1133–1152 (2013).
[Crossref] [PubMed]

B. J. Antony, M. D. Abràmoff, M. M. Harper, W. Jeong, E. H. Sohn, Y. H. Kwon, R. Kardon, and M. K. Garvin, “A combined machine-learning and graph-based framework for the segmentation of retinal surfaces in SD-OCT volumes,” Biomed. Opt. Express 4, 2712–2728 (2013).
[Crossref]

P. Barboni, V. Carelli, and G. Savini, “Microcystic macular degeneration from optic neuropathy: not inflammatory, not trans-synaptic degeneration,” Brain 136, e239 (2013).
[Crossref] [PubMed]

F. Kaufhold, H. Zimmermann, E. Schneider, K. Ruprecht, F. Paul, T. Oberwahrenbrock, and A. U. Brandt, “Optic neuritis is associated with inner nuclear layer thickening and microcystic macular edema independently of multiple sclerosis,” PLoS ONE 8, e71145 (2013).
[Crossref] [PubMed]

2012 (5)

X. Chen, M. Niemeijer, L. Zhang, K. Lee, M. Abramoff, and M. Sonka, “Three-dimensional segmentation of fluid-associated abnormalities in retinal OCT: probability constrained graph-search-graph-cut,” IEEE Trans. Med. Imag. 31, 1521–1531 (2012).
[Crossref]

S. J. Chiu, C. A. Toth, C. B. Rickman, J. A. Izatt, and S. Farsiu, “Automatic segmentation of closed-contour features in ophthalmic images using graph theory and dynamic programming,” Biomed. Opt. Express 3, 1127–1140 (2012).
[Crossref] [PubMed]

G. Wilkins, O. Houghton, and A. Oldenburg, “Automated segmentation of intraretinal cystoid fluid in optical coherence tomography,” IEEE Trans. Biomed. Eng. 59, 1109–1114 (2012).
[Crossref] [PubMed]

J. M. Gelfand, R. Nolan, D. M. Schwartz, J. Graves, and A. J. Green, “Microcystic macular oedema in multiple sclerosis is associated with disease severity,” Brain 135, 1786–1793 (2012).
[Crossref] [PubMed]

S. Saidha, E. S. Sotirchos, M. A. Ibrahim, C. M. Crainiceanu, J. M. Gelfand, Y. J. Sepah, J. N. Ratchford, J. Oh, M. A. Seigo, S. D. Newsome, L. J. Balcer, E. M. Frohman, A. J. Green, Q. D. Nguyen, and P. A. Calabresi, “Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study,” Lancet Neurol. 11, 963–972 (2012).
[Crossref] [PubMed]

2010 (2)

A. J. Green, S. McQuaid, S. L. Hauser, I. V. Allen, and R. Lyness, “Ocular pathology in multiple sclerosis: retinal atrophy and inflammation irrespective of disease duration,” Brain 133, 1591–1601 (2010).
[Crossref] [PubMed]

A. Petzold, J. F. de Boer, S. Schippling, P. Vermersch, R. Kardon, A. Green, P. A. Calabresi, and C. Polman, “Optical coherence tomography in multiple sclerosis: a systematic review and meta-analysis,” Lancet Neurol. 9, 921–932 (2010).
[Crossref] [PubMed]

2006 (1)

J. B. Fisher, D. A. Jacobs, C. E. Markowitz, S. L. Galetta, N. J. Volpe, M. L. Nano-Schiavi, M. L. Baier, E. M. Frohman, H. Winslow, T. C. Frohman, P. A. Calabresi, M. G. Maguire, G. R. Cutter, and L. J. Balcer, “Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis,” Ophthalmology 113, 324–332 (2006).
[Crossref] [PubMed]

2005 (1)

D. Fernandez, “Delineating fluid-filled region boundaries in optical coherence tomography images of the retina,” IEEE Trans. Med. Imag. 24, 929–945 (2005).
[Crossref]

2001 (1)

L. Breiman, “Random forests,” Machine Learning 45, 5–32 (2001).
[Crossref]

Abramoff, M.

X. Chen, M. Niemeijer, L. Zhang, K. Lee, M. Abramoff, and M. Sonka, “Three-dimensional segmentation of fluid-associated abnormalities in retinal OCT: probability constrained graph-search-graph-cut,” IEEE Trans. Med. Imag. 31, 1521–1531 (2012).
[Crossref]

Abràmoff, M. D.

B. J. Antony, M. D. Abràmoff, M. M. Harper, W. Jeong, E. H. Sohn, Y. H. Kwon, R. Kardon, and M. K. Garvin, “A combined machine-learning and graph-based framework for the segmentation of retinal surfaces in SD-OCT volumes,” Biomed. Opt. Express 4, 2712–2728 (2013).
[Crossref]

B. J. Antony, M. S. Miri, M. D. Abràmoff, Y. H. Kwon, and M. K. Garvin, “Automated 3D segmentation of multiple surfaces with a shared hole: segmentation of the neural canal opening in SD-OCT volumes,” in Proceedings of the International Conference on Medical Image Computing and Computer-Assisted Intervention, P. Golland, N. Hata, C. Barillot, J. Hornegger, and R. Howe, eds. (Springer, 2014), pp. 739–746.

Allen, I. V.

A. J. Green, S. McQuaid, S. L. Hauser, I. V. Allen, and R. Lyness, “Ocular pathology in multiple sclerosis: retinal atrophy and inflammation irrespective of disease duration,” Brain 133, 1591–1601 (2010).
[Crossref] [PubMed]

Antony, B. J.

B. J. Antony, M. D. Abràmoff, M. M. Harper, W. Jeong, E. H. Sohn, Y. H. Kwon, R. Kardon, and M. K. Garvin, “A combined machine-learning and graph-based framework for the segmentation of retinal surfaces in SD-OCT volumes,” Biomed. Opt. Express 4, 2712–2728 (2013).
[Crossref]

B. J. Antony, M. S. Miri, M. D. Abràmoff, Y. H. Kwon, and M. K. Garvin, “Automated 3D segmentation of multiple surfaces with a shared hole: segmentation of the neural canal opening in SD-OCT volumes,” in Proceedings of the International Conference on Medical Image Computing and Computer-Assisted Intervention, P. Golland, N. Hata, C. Barillot, J. Hornegger, and R. Howe, eds. (Springer, 2014), pp. 739–746.

Baier, M. L.

J. B. Fisher, D. A. Jacobs, C. E. Markowitz, S. L. Galetta, N. J. Volpe, M. L. Nano-Schiavi, M. L. Baier, E. M. Frohman, H. Winslow, T. C. Frohman, P. A. Calabresi, M. G. Maguire, G. R. Cutter, and L. J. Balcer, “Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis,” Ophthalmology 113, 324–332 (2006).
[Crossref] [PubMed]

Balcer, L. J.

J. N. Ratchford, S. Saidha, E. S. Sotirchos, J. A. Oh, M. A. Seigo, C. Eckstein, M. K. Durbin, J. D. Oakley, S. A. Meyer, A. Conger, T. C. Frohman, S. D. Newsome, L. J. Balcer, E. M. Frohman, and P. A. Calabresi, “Active MS is associated with accelerated retinal ganglion cell/inner plexiform layer thinning,” Neurology 80, 47–54 (2013).
[Crossref]

S. Saidha, E. S. Sotirchos, M. A. Ibrahim, C. M. Crainiceanu, J. M. Gelfand, Y. J. Sepah, J. N. Ratchford, J. Oh, M. A. Seigo, S. D. Newsome, L. J. Balcer, E. M. Frohman, A. J. Green, Q. D. Nguyen, and P. A. Calabresi, “Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study,” Lancet Neurol. 11, 963–972 (2012).
[Crossref] [PubMed]

J. B. Fisher, D. A. Jacobs, C. E. Markowitz, S. L. Galetta, N. J. Volpe, M. L. Nano-Schiavi, M. L. Baier, E. M. Frohman, H. Winslow, T. C. Frohman, P. A. Calabresi, M. G. Maguire, G. R. Cutter, and L. J. Balcer, “Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis,” Ophthalmology 113, 324–332 (2006).
[Crossref] [PubMed]

Balk, L.

M. C. Burggraaff, J. Trieu, W. A. E. J. de Vries-Knoppert, L. Balk, and A. Petzold, “The clinical spectrum of microcystic macular edema,” Invest. Ophthalmol. Vis. Sci. 55, 952–961 (2014).
[Crossref] [PubMed]

Barboni, P.

P. Barboni, V. Carelli, and G. Savini, “Microcystic macular degeneration from optic neuropathy: not inflammatory, not trans-synaptic degeneration,” Brain 136, e239 (2013).
[Crossref] [PubMed]

Bhargava, P.

P. Bhargava and P. A. Calabresi, “The expanding spectrum of aetiologies causing retinal microcystic macular change,” Brain 136, 3212–3214 (2013).
[Crossref] [PubMed]

Brandt, A. U.

F. Kaufhold, H. Zimmermann, E. Schneider, K. Ruprecht, F. Paul, T. Oberwahrenbrock, and A. U. Brandt, “Optic neuritis is associated with inner nuclear layer thickening and microcystic macular edema independently of multiple sclerosis,” PLoS ONE 8, e71145 (2013).
[Crossref] [PubMed]

Breiman, L.

L. Breiman, “Random forests,” Machine Learning 45, 5–32 (2001).
[Crossref]

Burggraaff, M. C.

M. C. Burggraaff, J. Trieu, W. A. E. J. de Vries-Knoppert, L. Balk, and A. Petzold, “The clinical spectrum of microcystic macular edema,” Invest. Ophthalmol. Vis. Sci. 55, 952–961 (2014).
[Crossref] [PubMed]

Calabresi, P. A.

E. K. Swingle, A. Lang, A. Carass, P. A. Calabresi, H. S. Ying, and J. L. Prince, “Microcystic macular edema detection in retina OCT images,” Proc. SPIE 9038, 90380O (2014).
[Crossref]

A. Lang, A. Carass, M. Hauser, E. S. Sotirchos, P. A. Calabresi, H. S. Ying, and J. L. Prince, “Retinal layer segmentation of macular OCT images using boundary classification,” Biomed. Opt. Express 4, 1133–1152 (2013).
[Crossref] [PubMed]

P. Bhargava and P. A. Calabresi, “The expanding spectrum of aetiologies causing retinal microcystic macular change,” Brain 136, 3212–3214 (2013).
[Crossref] [PubMed]

J. N. Ratchford, S. Saidha, E. S. Sotirchos, J. A. Oh, M. A. Seigo, C. Eckstein, M. K. Durbin, J. D. Oakley, S. A. Meyer, A. Conger, T. C. Frohman, S. D. Newsome, L. J. Balcer, E. M. Frohman, and P. A. Calabresi, “Active MS is associated with accelerated retinal ganglion cell/inner plexiform layer thinning,” Neurology 80, 47–54 (2013).
[Crossref]

S. Saidha, E. S. Sotirchos, M. A. Ibrahim, C. M. Crainiceanu, J. M. Gelfand, Y. J. Sepah, J. N. Ratchford, J. Oh, M. A. Seigo, S. D. Newsome, L. J. Balcer, E. M. Frohman, A. J. Green, Q. D. Nguyen, and P. A. Calabresi, “Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study,” Lancet Neurol. 11, 963–972 (2012).
[Crossref] [PubMed]

A. Petzold, J. F. de Boer, S. Schippling, P. Vermersch, R. Kardon, A. Green, P. A. Calabresi, and C. Polman, “Optical coherence tomography in multiple sclerosis: a systematic review and meta-analysis,” Lancet Neurol. 9, 921–932 (2010).
[Crossref] [PubMed]

J. B. Fisher, D. A. Jacobs, C. E. Markowitz, S. L. Galetta, N. J. Volpe, M. L. Nano-Schiavi, M. L. Baier, E. M. Frohman, H. Winslow, T. C. Frohman, P. A. Calabresi, M. G. Maguire, G. R. Cutter, and L. J. Balcer, “Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis,” Ophthalmology 113, 324–332 (2006).
[Crossref] [PubMed]

Campa, C.

Y. Zheng, J. Sahni, C. Campa, A. N. Stangos, A. Raj, and S. P. Harding, “Computerized assessment of intraretinal and subretinal fluid regions in spectral-domain optical coherence tomography images of the retina,” Am. J. Ophthalmol. 155, 277–286 (2013).
[Crossref]

Carass, A.

E. K. Swingle, A. Lang, A. Carass, P. A. Calabresi, H. S. Ying, and J. L. Prince, “Microcystic macular edema detection in retina OCT images,” Proc. SPIE 9038, 90380O (2014).
[Crossref]

A. Lang, A. Carass, M. Hauser, E. S. Sotirchos, P. A. Calabresi, H. S. Ying, and J. L. Prince, “Retinal layer segmentation of macular OCT images using boundary classification,” Biomed. Opt. Express 4, 1133–1152 (2013).
[Crossref] [PubMed]

Carelli, V.

P. Barboni, V. Carelli, and G. Savini, “Microcystic macular degeneration from optic neuropathy: not inflammatory, not trans-synaptic degeneration,” Brain 136, e239 (2013).
[Crossref] [PubMed]

Chen, X.

X. Chen, M. Niemeijer, L. Zhang, K. Lee, M. Abramoff, and M. Sonka, “Three-dimensional segmentation of fluid-associated abnormalities in retinal OCT: probability constrained graph-search-graph-cut,” IEEE Trans. Med. Imag. 31, 1521–1531 (2012).
[Crossref]

Chiu, S. J.

Conger, A.

J. N. Ratchford, S. Saidha, E. S. Sotirchos, J. A. Oh, M. A. Seigo, C. Eckstein, M. K. Durbin, J. D. Oakley, S. A. Meyer, A. Conger, T. C. Frohman, S. D. Newsome, L. J. Balcer, E. M. Frohman, and P. A. Calabresi, “Active MS is associated with accelerated retinal ganglion cell/inner plexiform layer thinning,” Neurology 80, 47–54 (2013).
[Crossref]

Crainiceanu, C. M.

S. Saidha, E. S. Sotirchos, M. A. Ibrahim, C. M. Crainiceanu, J. M. Gelfand, Y. J. Sepah, J. N. Ratchford, J. Oh, M. A. Seigo, S. D. Newsome, L. J. Balcer, E. M. Frohman, A. J. Green, Q. D. Nguyen, and P. A. Calabresi, “Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study,” Lancet Neurol. 11, 963–972 (2012).
[Crossref] [PubMed]

Cutter, G. R.

J. B. Fisher, D. A. Jacobs, C. E. Markowitz, S. L. Galetta, N. J. Volpe, M. L. Nano-Schiavi, M. L. Baier, E. M. Frohman, H. Winslow, T. C. Frohman, P. A. Calabresi, M. G. Maguire, G. R. Cutter, and L. J. Balcer, “Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis,” Ophthalmology 113, 324–332 (2006).
[Crossref] [PubMed]

de Boer, J. F.

A. Petzold, J. F. de Boer, S. Schippling, P. Vermersch, R. Kardon, A. Green, P. A. Calabresi, and C. Polman, “Optical coherence tomography in multiple sclerosis: a systematic review and meta-analysis,” Lancet Neurol. 9, 921–932 (2010).
[Crossref] [PubMed]

de Vries-Knoppert, W. A. E. J.

M. C. Burggraaff, J. Trieu, W. A. E. J. de Vries-Knoppert, L. Balk, and A. Petzold, “The clinical spectrum of microcystic macular edema,” Invest. Ophthalmol. Vis. Sci. 55, 952–961 (2014).
[Crossref] [PubMed]

De Zanet, S.

P. Dufour, S. De Zanet, U. Wolf-Schnurrbusch, and J. Kowal, “Classification of drusen positions in optical coherence tomography data from patients with age-related macular degeneration,” in Proceedings of the International Conference on Pattern Recognition, (IEEE, 2012), pp. 2067–2070.

Dufour, P.

P. Dufour, S. De Zanet, U. Wolf-Schnurrbusch, and J. Kowal, “Classification of drusen positions in optical coherence tomography data from patients with age-related macular degeneration,” in Proceedings of the International Conference on Pattern Recognition, (IEEE, 2012), pp. 2067–2070.

Durbin, M. K.

J. N. Ratchford, S. Saidha, E. S. Sotirchos, J. A. Oh, M. A. Seigo, C. Eckstein, M. K. Durbin, J. D. Oakley, S. A. Meyer, A. Conger, T. C. Frohman, S. D. Newsome, L. J. Balcer, E. M. Frohman, and P. A. Calabresi, “Active MS is associated with accelerated retinal ganglion cell/inner plexiform layer thinning,” Neurology 80, 47–54 (2013).
[Crossref]

Eckstein, C.

J. N. Ratchford, S. Saidha, E. S. Sotirchos, J. A. Oh, M. A. Seigo, C. Eckstein, M. K. Durbin, J. D. Oakley, S. A. Meyer, A. Conger, T. C. Frohman, S. D. Newsome, L. J. Balcer, E. M. Frohman, and P. A. Calabresi, “Active MS is associated with accelerated retinal ganglion cell/inner plexiform layer thinning,” Neurology 80, 47–54 (2013).
[Crossref]

Farsiu, S.

Fernandez, D.

D. Fernandez, “Delineating fluid-filled region boundaries in optical coherence tomography images of the retina,” IEEE Trans. Med. Imag. 24, 929–945 (2005).
[Crossref]

Fisher, J. B.

J. B. Fisher, D. A. Jacobs, C. E. Markowitz, S. L. Galetta, N. J. Volpe, M. L. Nano-Schiavi, M. L. Baier, E. M. Frohman, H. Winslow, T. C. Frohman, P. A. Calabresi, M. G. Maguire, G. R. Cutter, and L. J. Balcer, “Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis,” Ophthalmology 113, 324–332 (2006).
[Crossref] [PubMed]

Friedburg, C.

M. Pilch, K. Stieger, Y. Wenner, M. N. Preising, C. Friedburg, E. Meyer zu Bexten, and B. Lorenz, “Automated segmentation of pathological cavities in optical coherence tomography scans,” Invest. Ophthalmol. Vis. Sci. 54, 4385–4393 (2013).
[Crossref] [PubMed]

Frohman, E. M.

J. N. Ratchford, S. Saidha, E. S. Sotirchos, J. A. Oh, M. A. Seigo, C. Eckstein, M. K. Durbin, J. D. Oakley, S. A. Meyer, A. Conger, T. C. Frohman, S. D. Newsome, L. J. Balcer, E. M. Frohman, and P. A. Calabresi, “Active MS is associated with accelerated retinal ganglion cell/inner plexiform layer thinning,” Neurology 80, 47–54 (2013).
[Crossref]

S. Saidha, E. S. Sotirchos, M. A. Ibrahim, C. M. Crainiceanu, J. M. Gelfand, Y. J. Sepah, J. N. Ratchford, J. Oh, M. A. Seigo, S. D. Newsome, L. J. Balcer, E. M. Frohman, A. J. Green, Q. D. Nguyen, and P. A. Calabresi, “Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study,” Lancet Neurol. 11, 963–972 (2012).
[Crossref] [PubMed]

J. B. Fisher, D. A. Jacobs, C. E. Markowitz, S. L. Galetta, N. J. Volpe, M. L. Nano-Schiavi, M. L. Baier, E. M. Frohman, H. Winslow, T. C. Frohman, P. A. Calabresi, M. G. Maguire, G. R. Cutter, and L. J. Balcer, “Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis,” Ophthalmology 113, 324–332 (2006).
[Crossref] [PubMed]

Frohman, T. C.

J. N. Ratchford, S. Saidha, E. S. Sotirchos, J. A. Oh, M. A. Seigo, C. Eckstein, M. K. Durbin, J. D. Oakley, S. A. Meyer, A. Conger, T. C. Frohman, S. D. Newsome, L. J. Balcer, E. M. Frohman, and P. A. Calabresi, “Active MS is associated with accelerated retinal ganglion cell/inner plexiform layer thinning,” Neurology 80, 47–54 (2013).
[Crossref]

J. B. Fisher, D. A. Jacobs, C. E. Markowitz, S. L. Galetta, N. J. Volpe, M. L. Nano-Schiavi, M. L. Baier, E. M. Frohman, H. Winslow, T. C. Frohman, P. A. Calabresi, M. G. Maguire, G. R. Cutter, and L. J. Balcer, “Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis,” Ophthalmology 113, 324–332 (2006).
[Crossref] [PubMed]

Galetta, S. L.

J. B. Fisher, D. A. Jacobs, C. E. Markowitz, S. L. Galetta, N. J. Volpe, M. L. Nano-Schiavi, M. L. Baier, E. M. Frohman, H. Winslow, T. C. Frohman, P. A. Calabresi, M. G. Maguire, G. R. Cutter, and L. J. Balcer, “Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis,” Ophthalmology 113, 324–332 (2006).
[Crossref] [PubMed]

Garvin, M. K.

B. J. Antony, M. D. Abràmoff, M. M. Harper, W. Jeong, E. H. Sohn, Y. H. Kwon, R. Kardon, and M. K. Garvin, “A combined machine-learning and graph-based framework for the segmentation of retinal surfaces in SD-OCT volumes,” Biomed. Opt. Express 4, 2712–2728 (2013).
[Crossref]

B. J. Antony, M. S. Miri, M. D. Abràmoff, Y. H. Kwon, and M. K. Garvin, “Automated 3D segmentation of multiple surfaces with a shared hole: segmentation of the neural canal opening in SD-OCT volumes,” in Proceedings of the International Conference on Medical Image Computing and Computer-Assisted Intervention, P. Golland, N. Hata, C. Barillot, J. Hornegger, and R. Howe, eds. (Springer, 2014), pp. 739–746.

Gelfand, J. M.

J. M. Gelfand, R. Nolan, D. M. Schwartz, J. Graves, and A. J. Green, “Microcystic macular oedema in multiple sclerosis is associated with disease severity,” Brain 135, 1786–1793 (2012).
[Crossref] [PubMed]

S. Saidha, E. S. Sotirchos, M. A. Ibrahim, C. M. Crainiceanu, J. M. Gelfand, Y. J. Sepah, J. N. Ratchford, J. Oh, M. A. Seigo, S. D. Newsome, L. J. Balcer, E. M. Frohman, A. J. Green, Q. D. Nguyen, and P. A. Calabresi, “Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study,” Lancet Neurol. 11, 963–972 (2012).
[Crossref] [PubMed]

Graves, J.

J. M. Gelfand, R. Nolan, D. M. Schwartz, J. Graves, and A. J. Green, “Microcystic macular oedema in multiple sclerosis is associated with disease severity,” Brain 135, 1786–1793 (2012).
[Crossref] [PubMed]

Green, A.

A. Petzold, J. F. de Boer, S. Schippling, P. Vermersch, R. Kardon, A. Green, P. A. Calabresi, and C. Polman, “Optical coherence tomography in multiple sclerosis: a systematic review and meta-analysis,” Lancet Neurol. 9, 921–932 (2010).
[Crossref] [PubMed]

Green, A. J.

J. M. Gelfand, R. Nolan, D. M. Schwartz, J. Graves, and A. J. Green, “Microcystic macular oedema in multiple sclerosis is associated with disease severity,” Brain 135, 1786–1793 (2012).
[Crossref] [PubMed]

S. Saidha, E. S. Sotirchos, M. A. Ibrahim, C. M. Crainiceanu, J. M. Gelfand, Y. J. Sepah, J. N. Ratchford, J. Oh, M. A. Seigo, S. D. Newsome, L. J. Balcer, E. M. Frohman, A. J. Green, Q. D. Nguyen, and P. A. Calabresi, “Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study,” Lancet Neurol. 11, 963–972 (2012).
[Crossref] [PubMed]

A. J. Green, S. McQuaid, S. L. Hauser, I. V. Allen, and R. Lyness, “Ocular pathology in multiple sclerosis: retinal atrophy and inflammation irrespective of disease duration,” Brain 133, 1591–1601 (2010).
[Crossref] [PubMed]

Harding, S. P.

Y. Zheng, J. Sahni, C. Campa, A. N. Stangos, A. Raj, and S. P. Harding, “Computerized assessment of intraretinal and subretinal fluid regions in spectral-domain optical coherence tomography images of the retina,” Am. J. Ophthalmol. 155, 277–286 (2013).
[Crossref]

Harper, M. M.

Hauser, M.

Hauser, S. L.

A. J. Green, S. McQuaid, S. L. Hauser, I. V. Allen, and R. Lyness, “Ocular pathology in multiple sclerosis: retinal atrophy and inflammation irrespective of disease duration,” Brain 133, 1591–1601 (2010).
[Crossref] [PubMed]

Houghton, O.

G. Wilkins, O. Houghton, and A. Oldenburg, “Automated segmentation of intraretinal cystoid fluid in optical coherence tomography,” IEEE Trans. Biomed. Eng. 59, 1109–1114 (2012).
[Crossref] [PubMed]

Ibrahim, M. A.

S. Saidha, E. S. Sotirchos, M. A. Ibrahim, C. M. Crainiceanu, J. M. Gelfand, Y. J. Sepah, J. N. Ratchford, J. Oh, M. A. Seigo, S. D. Newsome, L. J. Balcer, E. M. Frohman, A. J. Green, Q. D. Nguyen, and P. A. Calabresi, “Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study,” Lancet Neurol. 11, 963–972 (2012).
[Crossref] [PubMed]

Izatt, J. A.

Jacobs, D. A.

J. B. Fisher, D. A. Jacobs, C. E. Markowitz, S. L. Galetta, N. J. Volpe, M. L. Nano-Schiavi, M. L. Baier, E. M. Frohman, H. Winslow, T. C. Frohman, P. A. Calabresi, M. G. Maguire, G. R. Cutter, and L. J. Balcer, “Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis,” Ophthalmology 113, 324–332 (2006).
[Crossref] [PubMed]

Jeong, W.

Kardon, R.

B. J. Antony, M. D. Abràmoff, M. M. Harper, W. Jeong, E. H. Sohn, Y. H. Kwon, R. Kardon, and M. K. Garvin, “A combined machine-learning and graph-based framework for the segmentation of retinal surfaces in SD-OCT volumes,” Biomed. Opt. Express 4, 2712–2728 (2013).
[Crossref]

A. Petzold, J. F. de Boer, S. Schippling, P. Vermersch, R. Kardon, A. Green, P. A. Calabresi, and C. Polman, “Optical coherence tomography in multiple sclerosis: a systematic review and meta-analysis,” Lancet Neurol. 9, 921–932 (2010).
[Crossref] [PubMed]

Kaufhold, F.

F. Kaufhold, H. Zimmermann, E. Schneider, K. Ruprecht, F. Paul, T. Oberwahrenbrock, and A. U. Brandt, “Optic neuritis is associated with inner nuclear layer thickening and microcystic macular edema independently of multiple sclerosis,” PLoS ONE 8, e71145 (2013).
[Crossref] [PubMed]

Kowal, J.

P. Dufour, S. De Zanet, U. Wolf-Schnurrbusch, and J. Kowal, “Classification of drusen positions in optical coherence tomography data from patients with age-related macular degeneration,” in Proceedings of the International Conference on Pattern Recognition, (IEEE, 2012), pp. 2067–2070.

Kwon, Y. H.

B. J. Antony, M. D. Abràmoff, M. M. Harper, W. Jeong, E. H. Sohn, Y. H. Kwon, R. Kardon, and M. K. Garvin, “A combined machine-learning and graph-based framework for the segmentation of retinal surfaces in SD-OCT volumes,” Biomed. Opt. Express 4, 2712–2728 (2013).
[Crossref]

B. J. Antony, M. S. Miri, M. D. Abràmoff, Y. H. Kwon, and M. K. Garvin, “Automated 3D segmentation of multiple surfaces with a shared hole: segmentation of the neural canal opening in SD-OCT volumes,” in Proceedings of the International Conference on Medical Image Computing and Computer-Assisted Intervention, P. Golland, N. Hata, C. Barillot, J. Hornegger, and R. Howe, eds. (Springer, 2014), pp. 739–746.

Lang, A.

E. K. Swingle, A. Lang, A. Carass, P. A. Calabresi, H. S. Ying, and J. L. Prince, “Microcystic macular edema detection in retina OCT images,” Proc. SPIE 9038, 90380O (2014).
[Crossref]

A. Lang, A. Carass, M. Hauser, E. S. Sotirchos, P. A. Calabresi, H. S. Ying, and J. L. Prince, “Retinal layer segmentation of macular OCT images using boundary classification,” Biomed. Opt. Express 4, 1133–1152 (2013).
[Crossref] [PubMed]

Lee, K.

X. Chen, M. Niemeijer, L. Zhang, K. Lee, M. Abramoff, and M. Sonka, “Three-dimensional segmentation of fluid-associated abnormalities in retinal OCT: probability constrained graph-search-graph-cut,” IEEE Trans. Med. Imag. 31, 1521–1531 (2012).
[Crossref]

Lorenz, B.

M. Pilch, K. Stieger, Y. Wenner, M. N. Preising, C. Friedburg, E. Meyer zu Bexten, and B. Lorenz, “Automated segmentation of pathological cavities in optical coherence tomography scans,” Invest. Ophthalmol. Vis. Sci. 54, 4385–4393 (2013).
[Crossref] [PubMed]

Lyness, R.

A. J. Green, S. McQuaid, S. L. Hauser, I. V. Allen, and R. Lyness, “Ocular pathology in multiple sclerosis: retinal atrophy and inflammation irrespective of disease duration,” Brain 133, 1591–1601 (2010).
[Crossref] [PubMed]

Maguire, M. G.

J. B. Fisher, D. A. Jacobs, C. E. Markowitz, S. L. Galetta, N. J. Volpe, M. L. Nano-Schiavi, M. L. Baier, E. M. Frohman, H. Winslow, T. C. Frohman, P. A. Calabresi, M. G. Maguire, G. R. Cutter, and L. J. Balcer, “Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis,” Ophthalmology 113, 324–332 (2006).
[Crossref] [PubMed]

Markowitz, C. E.

J. B. Fisher, D. A. Jacobs, C. E. Markowitz, S. L. Galetta, N. J. Volpe, M. L. Nano-Schiavi, M. L. Baier, E. M. Frohman, H. Winslow, T. C. Frohman, P. A. Calabresi, M. G. Maguire, G. R. Cutter, and L. J. Balcer, “Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis,” Ophthalmology 113, 324–332 (2006).
[Crossref] [PubMed]

McQuaid, S.

A. J. Green, S. McQuaid, S. L. Hauser, I. V. Allen, and R. Lyness, “Ocular pathology in multiple sclerosis: retinal atrophy and inflammation irrespective of disease duration,” Brain 133, 1591–1601 (2010).
[Crossref] [PubMed]

Meyer, S. A.

J. N. Ratchford, S. Saidha, E. S. Sotirchos, J. A. Oh, M. A. Seigo, C. Eckstein, M. K. Durbin, J. D. Oakley, S. A. Meyer, A. Conger, T. C. Frohman, S. D. Newsome, L. J. Balcer, E. M. Frohman, and P. A. Calabresi, “Active MS is associated with accelerated retinal ganglion cell/inner plexiform layer thinning,” Neurology 80, 47–54 (2013).
[Crossref]

Meyer zu Bexten, E.

M. Pilch, K. Stieger, Y. Wenner, M. N. Preising, C. Friedburg, E. Meyer zu Bexten, and B. Lorenz, “Automated segmentation of pathological cavities in optical coherence tomography scans,” Invest. Ophthalmol. Vis. Sci. 54, 4385–4393 (2013).
[Crossref] [PubMed]

Miri, M. S.

B. J. Antony, M. S. Miri, M. D. Abràmoff, Y. H. Kwon, and M. K. Garvin, “Automated 3D segmentation of multiple surfaces with a shared hole: segmentation of the neural canal opening in SD-OCT volumes,” in Proceedings of the International Conference on Medical Image Computing and Computer-Assisted Intervention, P. Golland, N. Hata, C. Barillot, J. Hornegger, and R. Howe, eds. (Springer, 2014), pp. 739–746.

Nano-Schiavi, M. L.

J. B. Fisher, D. A. Jacobs, C. E. Markowitz, S. L. Galetta, N. J. Volpe, M. L. Nano-Schiavi, M. L. Baier, E. M. Frohman, H. Winslow, T. C. Frohman, P. A. Calabresi, M. G. Maguire, G. R. Cutter, and L. J. Balcer, “Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis,” Ophthalmology 113, 324–332 (2006).
[Crossref] [PubMed]

Newsome, S. D.

J. N. Ratchford, S. Saidha, E. S. Sotirchos, J. A. Oh, M. A. Seigo, C. Eckstein, M. K. Durbin, J. D. Oakley, S. A. Meyer, A. Conger, T. C. Frohman, S. D. Newsome, L. J. Balcer, E. M. Frohman, and P. A. Calabresi, “Active MS is associated with accelerated retinal ganglion cell/inner plexiform layer thinning,” Neurology 80, 47–54 (2013).
[Crossref]

S. Saidha, E. S. Sotirchos, M. A. Ibrahim, C. M. Crainiceanu, J. M. Gelfand, Y. J. Sepah, J. N. Ratchford, J. Oh, M. A. Seigo, S. D. Newsome, L. J. Balcer, E. M. Frohman, A. J. Green, Q. D. Nguyen, and P. A. Calabresi, “Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study,” Lancet Neurol. 11, 963–972 (2012).
[Crossref] [PubMed]

Nguyen, Q. D.

S. Saidha, E. S. Sotirchos, M. A. Ibrahim, C. M. Crainiceanu, J. M. Gelfand, Y. J. Sepah, J. N. Ratchford, J. Oh, M. A. Seigo, S. D. Newsome, L. J. Balcer, E. M. Frohman, A. J. Green, Q. D. Nguyen, and P. A. Calabresi, “Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study,” Lancet Neurol. 11, 963–972 (2012).
[Crossref] [PubMed]

Niemeijer, M.

X. Chen, M. Niemeijer, L. Zhang, K. Lee, M. Abramoff, and M. Sonka, “Three-dimensional segmentation of fluid-associated abnormalities in retinal OCT: probability constrained graph-search-graph-cut,” IEEE Trans. Med. Imag. 31, 1521–1531 (2012).
[Crossref]

Nolan, R.

J. M. Gelfand, R. Nolan, D. M. Schwartz, J. Graves, and A. J. Green, “Microcystic macular oedema in multiple sclerosis is associated with disease severity,” Brain 135, 1786–1793 (2012).
[Crossref] [PubMed]

Oakley, J. D.

J. N. Ratchford, S. Saidha, E. S. Sotirchos, J. A. Oh, M. A. Seigo, C. Eckstein, M. K. Durbin, J. D. Oakley, S. A. Meyer, A. Conger, T. C. Frohman, S. D. Newsome, L. J. Balcer, E. M. Frohman, and P. A. Calabresi, “Active MS is associated with accelerated retinal ganglion cell/inner plexiform layer thinning,” Neurology 80, 47–54 (2013).
[Crossref]

Oberwahrenbrock, T.

F. Kaufhold, H. Zimmermann, E. Schneider, K. Ruprecht, F. Paul, T. Oberwahrenbrock, and A. U. Brandt, “Optic neuritis is associated with inner nuclear layer thickening and microcystic macular edema independently of multiple sclerosis,” PLoS ONE 8, e71145 (2013).
[Crossref] [PubMed]

Oh, J.

S. Saidha, E. S. Sotirchos, M. A. Ibrahim, C. M. Crainiceanu, J. M. Gelfand, Y. J. Sepah, J. N. Ratchford, J. Oh, M. A. Seigo, S. D. Newsome, L. J. Balcer, E. M. Frohman, A. J. Green, Q. D. Nguyen, and P. A. Calabresi, “Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study,” Lancet Neurol. 11, 963–972 (2012).
[Crossref] [PubMed]

Oh, J. A.

J. N. Ratchford, S. Saidha, E. S. Sotirchos, J. A. Oh, M. A. Seigo, C. Eckstein, M. K. Durbin, J. D. Oakley, S. A. Meyer, A. Conger, T. C. Frohman, S. D. Newsome, L. J. Balcer, E. M. Frohman, and P. A. Calabresi, “Active MS is associated with accelerated retinal ganglion cell/inner plexiform layer thinning,” Neurology 80, 47–54 (2013).
[Crossref]

Oldenburg, A.

G. Wilkins, O. Houghton, and A. Oldenburg, “Automated segmentation of intraretinal cystoid fluid in optical coherence tomography,” IEEE Trans. Biomed. Eng. 59, 1109–1114 (2012).
[Crossref] [PubMed]

Paul, F.

F. Kaufhold, H. Zimmermann, E. Schneider, K. Ruprecht, F. Paul, T. Oberwahrenbrock, and A. U. Brandt, “Optic neuritis is associated with inner nuclear layer thickening and microcystic macular edema independently of multiple sclerosis,” PLoS ONE 8, e71145 (2013).
[Crossref] [PubMed]

Petzold, A.

M. C. Burggraaff, J. Trieu, W. A. E. J. de Vries-Knoppert, L. Balk, and A. Petzold, “The clinical spectrum of microcystic macular edema,” Invest. Ophthalmol. Vis. Sci. 55, 952–961 (2014).
[Crossref] [PubMed]

A. Petzold, J. F. de Boer, S. Schippling, P. Vermersch, R. Kardon, A. Green, P. A. Calabresi, and C. Polman, “Optical coherence tomography in multiple sclerosis: a systematic review and meta-analysis,” Lancet Neurol. 9, 921–932 (2010).
[Crossref] [PubMed]

Pilch, M.

M. Pilch, K. Stieger, Y. Wenner, M. N. Preising, C. Friedburg, E. Meyer zu Bexten, and B. Lorenz, “Automated segmentation of pathological cavities in optical coherence tomography scans,” Invest. Ophthalmol. Vis. Sci. 54, 4385–4393 (2013).
[Crossref] [PubMed]

Polman, C.

A. Petzold, J. F. de Boer, S. Schippling, P. Vermersch, R. Kardon, A. Green, P. A. Calabresi, and C. Polman, “Optical coherence tomography in multiple sclerosis: a systematic review and meta-analysis,” Lancet Neurol. 9, 921–932 (2010).
[Crossref] [PubMed]

Preising, M. N.

M. Pilch, K. Stieger, Y. Wenner, M. N. Preising, C. Friedburg, E. Meyer zu Bexten, and B. Lorenz, “Automated segmentation of pathological cavities in optical coherence tomography scans,” Invest. Ophthalmol. Vis. Sci. 54, 4385–4393 (2013).
[Crossref] [PubMed]

Prince, J. L.

E. K. Swingle, A. Lang, A. Carass, P. A. Calabresi, H. S. Ying, and J. L. Prince, “Microcystic macular edema detection in retina OCT images,” Proc. SPIE 9038, 90380O (2014).
[Crossref]

A. Lang, A. Carass, M. Hauser, E. S. Sotirchos, P. A. Calabresi, H. S. Ying, and J. L. Prince, “Retinal layer segmentation of macular OCT images using boundary classification,” Biomed. Opt. Express 4, 1133–1152 (2013).
[Crossref] [PubMed]

Raj, A.

Y. Zheng, J. Sahni, C. Campa, A. N. Stangos, A. Raj, and S. P. Harding, “Computerized assessment of intraretinal and subretinal fluid regions in spectral-domain optical coherence tomography images of the retina,” Am. J. Ophthalmol. 155, 277–286 (2013).
[Crossref]

Ratchford, J. N.

J. N. Ratchford, S. Saidha, E. S. Sotirchos, J. A. Oh, M. A. Seigo, C. Eckstein, M. K. Durbin, J. D. Oakley, S. A. Meyer, A. Conger, T. C. Frohman, S. D. Newsome, L. J. Balcer, E. M. Frohman, and P. A. Calabresi, “Active MS is associated with accelerated retinal ganglion cell/inner plexiform layer thinning,” Neurology 80, 47–54 (2013).
[Crossref]

S. Saidha, E. S. Sotirchos, M. A. Ibrahim, C. M. Crainiceanu, J. M. Gelfand, Y. J. Sepah, J. N. Ratchford, J. Oh, M. A. Seigo, S. D. Newsome, L. J. Balcer, E. M. Frohman, A. J. Green, Q. D. Nguyen, and P. A. Calabresi, “Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study,” Lancet Neurol. 11, 963–972 (2012).
[Crossref] [PubMed]

Rickman, C. B.

Ruprecht, K.

F. Kaufhold, H. Zimmermann, E. Schneider, K. Ruprecht, F. Paul, T. Oberwahrenbrock, and A. U. Brandt, “Optic neuritis is associated with inner nuclear layer thickening and microcystic macular edema independently of multiple sclerosis,” PLoS ONE 8, e71145 (2013).
[Crossref] [PubMed]

Sahni, J.

Y. Zheng, J. Sahni, C. Campa, A. N. Stangos, A. Raj, and S. P. Harding, “Computerized assessment of intraretinal and subretinal fluid regions in spectral-domain optical coherence tomography images of the retina,” Am. J. Ophthalmol. 155, 277–286 (2013).
[Crossref]

Saidha, S.

J. N. Ratchford, S. Saidha, E. S. Sotirchos, J. A. Oh, M. A. Seigo, C. Eckstein, M. K. Durbin, J. D. Oakley, S. A. Meyer, A. Conger, T. C. Frohman, S. D. Newsome, L. J. Balcer, E. M. Frohman, and P. A. Calabresi, “Active MS is associated with accelerated retinal ganglion cell/inner plexiform layer thinning,” Neurology 80, 47–54 (2013).
[Crossref]

S. Saidha, E. S. Sotirchos, M. A. Ibrahim, C. M. Crainiceanu, J. M. Gelfand, Y. J. Sepah, J. N. Ratchford, J. Oh, M. A. Seigo, S. D. Newsome, L. J. Balcer, E. M. Frohman, A. J. Green, Q. D. Nguyen, and P. A. Calabresi, “Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study,” Lancet Neurol. 11, 963–972 (2012).
[Crossref] [PubMed]

Savini, G.

P. Barboni, V. Carelli, and G. Savini, “Microcystic macular degeneration from optic neuropathy: not inflammatory, not trans-synaptic degeneration,” Brain 136, e239 (2013).
[Crossref] [PubMed]

Schippling, S.

A. Petzold, J. F. de Boer, S. Schippling, P. Vermersch, R. Kardon, A. Green, P. A. Calabresi, and C. Polman, “Optical coherence tomography in multiple sclerosis: a systematic review and meta-analysis,” Lancet Neurol. 9, 921–932 (2010).
[Crossref] [PubMed]

Schneider, E.

F. Kaufhold, H. Zimmermann, E. Schneider, K. Ruprecht, F. Paul, T. Oberwahrenbrock, and A. U. Brandt, “Optic neuritis is associated with inner nuclear layer thickening and microcystic macular edema independently of multiple sclerosis,” PLoS ONE 8, e71145 (2013).
[Crossref] [PubMed]

Schwartz, D. M.

J. M. Gelfand, R. Nolan, D. M. Schwartz, J. Graves, and A. J. Green, “Microcystic macular oedema in multiple sclerosis is associated with disease severity,” Brain 135, 1786–1793 (2012).
[Crossref] [PubMed]

Seigo, M. A.

J. N. Ratchford, S. Saidha, E. S. Sotirchos, J. A. Oh, M. A. Seigo, C. Eckstein, M. K. Durbin, J. D. Oakley, S. A. Meyer, A. Conger, T. C. Frohman, S. D. Newsome, L. J. Balcer, E. M. Frohman, and P. A. Calabresi, “Active MS is associated with accelerated retinal ganglion cell/inner plexiform layer thinning,” Neurology 80, 47–54 (2013).
[Crossref]

S. Saidha, E. S. Sotirchos, M. A. Ibrahim, C. M. Crainiceanu, J. M. Gelfand, Y. J. Sepah, J. N. Ratchford, J. Oh, M. A. Seigo, S. D. Newsome, L. J. Balcer, E. M. Frohman, A. J. Green, Q. D. Nguyen, and P. A. Calabresi, “Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study,” Lancet Neurol. 11, 963–972 (2012).
[Crossref] [PubMed]

Sepah, Y. J.

S. Saidha, E. S. Sotirchos, M. A. Ibrahim, C. M. Crainiceanu, J. M. Gelfand, Y. J. Sepah, J. N. Ratchford, J. Oh, M. A. Seigo, S. D. Newsome, L. J. Balcer, E. M. Frohman, A. J. Green, Q. D. Nguyen, and P. A. Calabresi, “Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study,” Lancet Neurol. 11, 963–972 (2012).
[Crossref] [PubMed]

Sohn, E. H.

Sonka, M.

X. Chen, M. Niemeijer, L. Zhang, K. Lee, M. Abramoff, and M. Sonka, “Three-dimensional segmentation of fluid-associated abnormalities in retinal OCT: probability constrained graph-search-graph-cut,” IEEE Trans. Med. Imag. 31, 1521–1531 (2012).
[Crossref]

Sotirchos, E. S.

A. Lang, A. Carass, M. Hauser, E. S. Sotirchos, P. A. Calabresi, H. S. Ying, and J. L. Prince, “Retinal layer segmentation of macular OCT images using boundary classification,” Biomed. Opt. Express 4, 1133–1152 (2013).
[Crossref] [PubMed]

J. N. Ratchford, S. Saidha, E. S. Sotirchos, J. A. Oh, M. A. Seigo, C. Eckstein, M. K. Durbin, J. D. Oakley, S. A. Meyer, A. Conger, T. C. Frohman, S. D. Newsome, L. J. Balcer, E. M. Frohman, and P. A. Calabresi, “Active MS is associated with accelerated retinal ganglion cell/inner plexiform layer thinning,” Neurology 80, 47–54 (2013).
[Crossref]

S. Saidha, E. S. Sotirchos, M. A. Ibrahim, C. M. Crainiceanu, J. M. Gelfand, Y. J. Sepah, J. N. Ratchford, J. Oh, M. A. Seigo, S. D. Newsome, L. J. Balcer, E. M. Frohman, A. J. Green, Q. D. Nguyen, and P. A. Calabresi, “Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study,” Lancet Neurol. 11, 963–972 (2012).
[Crossref] [PubMed]

Stangos, A. N.

Y. Zheng, J. Sahni, C. Campa, A. N. Stangos, A. Raj, and S. P. Harding, “Computerized assessment of intraretinal and subretinal fluid regions in spectral-domain optical coherence tomography images of the retina,” Am. J. Ophthalmol. 155, 277–286 (2013).
[Crossref]

Stieger, K.

M. Pilch, K. Stieger, Y. Wenner, M. N. Preising, C. Friedburg, E. Meyer zu Bexten, and B. Lorenz, “Automated segmentation of pathological cavities in optical coherence tomography scans,” Invest. Ophthalmol. Vis. Sci. 54, 4385–4393 (2013).
[Crossref] [PubMed]

Swingle, E. K.

E. K. Swingle, A. Lang, A. Carass, P. A. Calabresi, H. S. Ying, and J. L. Prince, “Microcystic macular edema detection in retina OCT images,” Proc. SPIE 9038, 90380O (2014).
[Crossref]

Toth, C. A.

Trieu, J.

M. C. Burggraaff, J. Trieu, W. A. E. J. de Vries-Knoppert, L. Balk, and A. Petzold, “The clinical spectrum of microcystic macular edema,” Invest. Ophthalmol. Vis. Sci. 55, 952–961 (2014).
[Crossref] [PubMed]

Vermersch, P.

A. Petzold, J. F. de Boer, S. Schippling, P. Vermersch, R. Kardon, A. Green, P. A. Calabresi, and C. Polman, “Optical coherence tomography in multiple sclerosis: a systematic review and meta-analysis,” Lancet Neurol. 9, 921–932 (2010).
[Crossref] [PubMed]

Volpe, N. J.

J. B. Fisher, D. A. Jacobs, C. E. Markowitz, S. L. Galetta, N. J. Volpe, M. L. Nano-Schiavi, M. L. Baier, E. M. Frohman, H. Winslow, T. C. Frohman, P. A. Calabresi, M. G. Maguire, G. R. Cutter, and L. J. Balcer, “Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis,” Ophthalmology 113, 324–332 (2006).
[Crossref] [PubMed]

Wenner, Y.

M. Pilch, K. Stieger, Y. Wenner, M. N. Preising, C. Friedburg, E. Meyer zu Bexten, and B. Lorenz, “Automated segmentation of pathological cavities in optical coherence tomography scans,” Invest. Ophthalmol. Vis. Sci. 54, 4385–4393 (2013).
[Crossref] [PubMed]

Wilkins, G.

G. Wilkins, O. Houghton, and A. Oldenburg, “Automated segmentation of intraretinal cystoid fluid in optical coherence tomography,” IEEE Trans. Biomed. Eng. 59, 1109–1114 (2012).
[Crossref] [PubMed]

Winslow, H.

J. B. Fisher, D. A. Jacobs, C. E. Markowitz, S. L. Galetta, N. J. Volpe, M. L. Nano-Schiavi, M. L. Baier, E. M. Frohman, H. Winslow, T. C. Frohman, P. A. Calabresi, M. G. Maguire, G. R. Cutter, and L. J. Balcer, “Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis,” Ophthalmology 113, 324–332 (2006).
[Crossref] [PubMed]

Wolf-Schnurrbusch, U.

P. Dufour, S. De Zanet, U. Wolf-Schnurrbusch, and J. Kowal, “Classification of drusen positions in optical coherence tomography data from patients with age-related macular degeneration,” in Proceedings of the International Conference on Pattern Recognition, (IEEE, 2012), pp. 2067–2070.

Ying, H. S.

E. K. Swingle, A. Lang, A. Carass, P. A. Calabresi, H. S. Ying, and J. L. Prince, “Microcystic macular edema detection in retina OCT images,” Proc. SPIE 9038, 90380O (2014).
[Crossref]

A. Lang, A. Carass, M. Hauser, E. S. Sotirchos, P. A. Calabresi, H. S. Ying, and J. L. Prince, “Retinal layer segmentation of macular OCT images using boundary classification,” Biomed. Opt. Express 4, 1133–1152 (2013).
[Crossref] [PubMed]

Zhang, L.

X. Chen, M. Niemeijer, L. Zhang, K. Lee, M. Abramoff, and M. Sonka, “Three-dimensional segmentation of fluid-associated abnormalities in retinal OCT: probability constrained graph-search-graph-cut,” IEEE Trans. Med. Imag. 31, 1521–1531 (2012).
[Crossref]

Zheng, Y.

Y. Zheng, J. Sahni, C. Campa, A. N. Stangos, A. Raj, and S. P. Harding, “Computerized assessment of intraretinal and subretinal fluid regions in spectral-domain optical coherence tomography images of the retina,” Am. J. Ophthalmol. 155, 277–286 (2013).
[Crossref]

Zimmermann, H.

F. Kaufhold, H. Zimmermann, E. Schneider, K. Ruprecht, F. Paul, T. Oberwahrenbrock, and A. U. Brandt, “Optic neuritis is associated with inner nuclear layer thickening and microcystic macular edema independently of multiple sclerosis,” PLoS ONE 8, e71145 (2013).
[Crossref] [PubMed]

Am. J. Ophthalmol. (1)

Y. Zheng, J. Sahni, C. Campa, A. N. Stangos, A. Raj, and S. P. Harding, “Computerized assessment of intraretinal and subretinal fluid regions in spectral-domain optical coherence tomography images of the retina,” Am. J. Ophthalmol. 155, 277–286 (2013).
[Crossref]

Biomed. Opt. Express (3)

Brain (4)

A. J. Green, S. McQuaid, S. L. Hauser, I. V. Allen, and R. Lyness, “Ocular pathology in multiple sclerosis: retinal atrophy and inflammation irrespective of disease duration,” Brain 133, 1591–1601 (2010).
[Crossref] [PubMed]

J. M. Gelfand, R. Nolan, D. M. Schwartz, J. Graves, and A. J. Green, “Microcystic macular oedema in multiple sclerosis is associated with disease severity,” Brain 135, 1786–1793 (2012).
[Crossref] [PubMed]

P. Barboni, V. Carelli, and G. Savini, “Microcystic macular degeneration from optic neuropathy: not inflammatory, not trans-synaptic degeneration,” Brain 136, e239 (2013).
[Crossref] [PubMed]

P. Bhargava and P. A. Calabresi, “The expanding spectrum of aetiologies causing retinal microcystic macular change,” Brain 136, 3212–3214 (2013).
[Crossref] [PubMed]

IEEE Trans. Biomed. Eng. (1)

G. Wilkins, O. Houghton, and A. Oldenburg, “Automated segmentation of intraretinal cystoid fluid in optical coherence tomography,” IEEE Trans. Biomed. Eng. 59, 1109–1114 (2012).
[Crossref] [PubMed]

IEEE Trans. Med. Imag. (2)

X. Chen, M. Niemeijer, L. Zhang, K. Lee, M. Abramoff, and M. Sonka, “Three-dimensional segmentation of fluid-associated abnormalities in retinal OCT: probability constrained graph-search-graph-cut,” IEEE Trans. Med. Imag. 31, 1521–1531 (2012).
[Crossref]

D. Fernandez, “Delineating fluid-filled region boundaries in optical coherence tomography images of the retina,” IEEE Trans. Med. Imag. 24, 929–945 (2005).
[Crossref]

Invest. Ophthalmol. Vis. Sci. (2)

M. C. Burggraaff, J. Trieu, W. A. E. J. de Vries-Knoppert, L. Balk, and A. Petzold, “The clinical spectrum of microcystic macular edema,” Invest. Ophthalmol. Vis. Sci. 55, 952–961 (2014).
[Crossref] [PubMed]

M. Pilch, K. Stieger, Y. Wenner, M. N. Preising, C. Friedburg, E. Meyer zu Bexten, and B. Lorenz, “Automated segmentation of pathological cavities in optical coherence tomography scans,” Invest. Ophthalmol. Vis. Sci. 54, 4385–4393 (2013).
[Crossref] [PubMed]

Lancet Neurol. (2)

S. Saidha, E. S. Sotirchos, M. A. Ibrahim, C. M. Crainiceanu, J. M. Gelfand, Y. J. Sepah, J. N. Ratchford, J. Oh, M. A. Seigo, S. D. Newsome, L. J. Balcer, E. M. Frohman, A. J. Green, Q. D. Nguyen, and P. A. Calabresi, “Microcystic macular oedema, thickness of the inner nuclear layer of the retina, and disease characteristics in multiple sclerosis: a retrospective study,” Lancet Neurol. 11, 963–972 (2012).
[Crossref] [PubMed]

A. Petzold, J. F. de Boer, S. Schippling, P. Vermersch, R. Kardon, A. Green, P. A. Calabresi, and C. Polman, “Optical coherence tomography in multiple sclerosis: a systematic review and meta-analysis,” Lancet Neurol. 9, 921–932 (2010).
[Crossref] [PubMed]

Machine Learning (1)

L. Breiman, “Random forests,” Machine Learning 45, 5–32 (2001).
[Crossref]

Neurology (1)

J. N. Ratchford, S. Saidha, E. S. Sotirchos, J. A. Oh, M. A. Seigo, C. Eckstein, M. K. Durbin, J. D. Oakley, S. A. Meyer, A. Conger, T. C. Frohman, S. D. Newsome, L. J. Balcer, E. M. Frohman, and P. A. Calabresi, “Active MS is associated with accelerated retinal ganglion cell/inner plexiform layer thinning,” Neurology 80, 47–54 (2013).
[Crossref]

Ophthalmology (1)

J. B. Fisher, D. A. Jacobs, C. E. Markowitz, S. L. Galetta, N. J. Volpe, M. L. Nano-Schiavi, M. L. Baier, E. M. Frohman, H. Winslow, T. C. Frohman, P. A. Calabresi, M. G. Maguire, G. R. Cutter, and L. J. Balcer, “Relation of visual function to retinal nerve fiber layer thickness in multiple sclerosis,” Ophthalmology 113, 324–332 (2006).
[Crossref] [PubMed]

PLoS ONE (1)

F. Kaufhold, H. Zimmermann, E. Schneider, K. Ruprecht, F. Paul, T. Oberwahrenbrock, and A. U. Brandt, “Optic neuritis is associated with inner nuclear layer thickening and microcystic macular edema independently of multiple sclerosis,” PLoS ONE 8, e71145 (2013).
[Crossref] [PubMed]

Proc. SPIE (1)

E. K. Swingle, A. Lang, A. Carass, P. A. Calabresi, H. S. Ying, and J. L. Prince, “Microcystic macular edema detection in retina OCT images,” Proc. SPIE 9038, 90380O (2014).
[Crossref]

Other (2)

B. J. Antony, M. S. Miri, M. D. Abràmoff, Y. H. Kwon, and M. K. Garvin, “Automated 3D segmentation of multiple surfaces with a shared hole: segmentation of the neural canal opening in SD-OCT volumes,” in Proceedings of the International Conference on Medical Image Computing and Computer-Assisted Intervention, P. Golland, N. Hata, C. Barillot, J. Hornegger, and R. Howe, eds. (Springer, 2014), pp. 739–746.

P. Dufour, S. De Zanet, U. Wolf-Schnurrbusch, and J. Kowal, “Classification of drusen positions in optical coherence tomography data from patients with age-related macular degeneration,” in Proceedings of the International Conference on Pattern Recognition, (IEEE, 2012), pp. 2067–2070.

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Figures (5)

Fig. 1
Fig. 1 B-scan images and corresponding pseudocyst manual segmentations from two different subjects. The averaging done by the scanner makes the pseudocysts in (b) more difficult to distinguish.
Fig. 2
Fig. 2 (a) B-scan images before and after intensity normalization. The dashed lines in the original image represent the area used to compute the fundus projection image (FPI) shown in (b). (b) Estimation of the bias field and its decomposition into two components using the FPI. The green line on the FPI shows where the B-scan in (a) was acquired.
Fig. 3
Fig. 3 Example images for several of the features used by the classifier to find the MME. The SNR feature is not shown since it was fairly uniform for this subject.
Fig. 4
Fig. 4 B-scan images showing the original images and those with the results overlaid. The algorithm is shown in red, the manual segmentation in green, and the agreement of the two in blue. Images (a) and (b) are from low pseudocyst density subjects while (c) and (d) are from high density subjects.
Fig. 5
Fig. 5 Plot of the median F-measure, precision, and recall values over all scans for varying values of the high probability threshold. The maximum F-measure value was used to determine the final threshold.

Tables (5)

Tables Icon

Table 1 Overview of the data used for this study including the statistics of the pseudocysts as labeled by the first manual rater. (OD - right eye, OS - left eye)

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Table 2 List of the 18 features used by the random forest classifier.

Tables Icon

Table 3 Median precision, recall, and F-measure values over all cross-validation runs with IQR in parentheses.

Tables Icon

Table 4 The total difference in number of pseudocysts found and the overall difference in MME volume. Differences were computed as (algorithm − truth). Values represent the median over all scans with IQR in parentheses.

Tables Icon

Table 5 The results of running the algorithm on non-MME data. Shown are the total number of estimated pseudocysts found and the total MME volume.

Equations (2)

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I ^ ( x , y , z ) = I ( x , y , z ) N ( x , y ) ,
Pr = TP TP + FP = # correct # found Re = TP TP + FN = # correct # true F-m = 2 Pr Re Pr + Re

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