Abstract

Scanning laser ophthalmoscopes (SLOs) are able to achieve superior contrast and axial sectioning capability compared to fundus photography. However, SLOs typically use monochromatic illumination and are thus unable to extract color information of the retina. Previous color SLO imaging techniques utilized multiple lasers or narrow band sources for illumination, which allowed for multiple color but not “true color” imaging as done in fundus photography. We describe the first “true color” SLO, handheld color SLO, and combined color SLO integrated with a spectral domain optical coherence tomography (OCT) system. To achieve accurate color imaging, the SLO was calibrated with a color test target and utilized an achromatizing lens when imaging the retina to correct for the eye’s longitudinal chromatic aberration. Color SLO and OCT images from volunteers were then acquired simultaneously with a combined power under the ANSI limit. Images from this system were then compared with those from commercially available SLOs featuring multiple narrow-band color imaging.

© 2014 Optical Society of America

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2014 (1)

2013 (3)

2012 (1)

2011 (4)

2010 (2)

2008 (1)

2007 (3)

2006 (2)

2005 (3)

D. A. Atchison and G. Smith, “Chromatic dispersions of the ocular media of human eyes,” J. Opt. Soc. Am. A22(1), 29–37 (2005).
[CrossRef] [PubMed]

S. S. Ahmed, M. N. Lott, and D. M. Marcus, “The macular xanthophylls,” Surv. Ophthalmol.50(2), 183–193 (2005).
[CrossRef] [PubMed]

D. X. Hammer, N. V. Iftimia, T. E. Ustun, J. C. Magill, and R. D. Ferguson, “Dual OCT/SLO imager with three-dimensional tracker,” Proc. SPIE5688, 33–44 (2005).
[CrossRef]

2002 (2)

P. Vieira, A. Manivannan, P. F. Sharp, and J. V. Forrester, “True colour imaging of the fundus using a scanning laser ophthalmoscope,” Physiol. Meas.23(1), 1–10 (2002).
[CrossRef] [PubMed]

D. U. Bartsch, W. R. Freeman, and A. M. Lopez, “A false use of “true color”,” Arch. Ophthalmol.120(5), 675–676 (2002).
[PubMed]

2001 (2)

R. A. Ashman, F. Reinholz, and R. H. Eikelboom, “Improvements in Colour Fundus Imaging Using Scanning Laser Ophthalmoscopy,” Lasers Med. Sci.16(1), 52–59 (2001).
[CrossRef] [PubMed]

A. Manivannan, J. Van der Hoek, P. Vieira, A. Farrow, J. Olson, P. F. Sharp, and J. V. Forrester, “Clinical investigation of a true color scanning laser ophthalmoscope,” Arch. Ophthalmol.119(6), 819–824 (2001).
[CrossRef] [PubMed]

1999 (1)

F. Reinholz, R. A. Ashman, and R. H. Eikelboom, “Simultaneous three wavelength imaging with a scanning laser ophthalmoscope,” Cytometry37(3), 165–170 (1999).
[CrossRef] [PubMed]

1998 (2)

A. Manivannan, J. N. P. Kirkpatrick, P. F. Sharp, and J. V. Forrester, “Novel approach towards colour imaging using a scanning laser ophthalmoscope,” Br. J. Ophthalmol.82(4), 342–345 (1998).
[CrossRef] [PubMed]

A. G. Podoleanu and D. A. Jackson, “Combined optical coherence tomograph and scanning laser ophthalmoscope,” Electron. Lett.34(11), 1088–1090 (1998).
[CrossRef]

1991 (1)

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

1989 (1)

1987 (1)

1982 (1)

A. L. Lewis, M. Katz, and C. Oehrlein, “A modified achromatizing lens,” Am. J. Optom. Physiol. Opt.59(11), 909–911 (1982).
[CrossRef] [PubMed]

1981 (1)

1976 (1)

K. McLaren, “XIII—The Development of the CIE 1976 (L* a* b*) Uniform Colour Space and Colour-difference Formula,” J. Soc. Dyers Colourists92(9), 338–341 (1976).
[CrossRef]

1957 (1)

1946 (1)

Ahmed, S. S.

S. S. Ahmed, M. N. Lott, and D. M. Marcus, “The macular xanthophylls,” Surv. Ophthalmol.50(2), 183–193 (2005).
[CrossRef] [PubMed]

Arathorn, D. W.

Artal, P.

Ashman, R. A.

R. A. Ashman, F. Reinholz, and R. H. Eikelboom, “Improvements in Colour Fundus Imaging Using Scanning Laser Ophthalmoscopy,” Lasers Med. Sci.16(1), 52–59 (2001).
[CrossRef] [PubMed]

F. Reinholz, R. A. Ashman, and R. H. Eikelboom, “Simultaneous three wavelength imaging with a scanning laser ophthalmoscope,” Cytometry37(3), 165–170 (1999).
[CrossRef] [PubMed]

Atchison, D. A.

Balderas-Mata, S.

Bartsch, D. U.

D. U. Bartsch, W. R. Freeman, and A. M. Lopez, “A false use of “true color”,” Arch. Ophthalmol.120(5), 675–676 (2002).
[PubMed]

Bedford, R. E.

Benny, Y.

Braaf, B.

Bradu, A.

Cense, B.

Chang, W.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Choi, S. S.

Chow, L. P.

S. P. Hibbs, A. Smith, L. P. Chow, and S. M. Downes, “Colour photographs for screening in neovascular age-related macular degeneration: are they necessary?” Eye (Lond.)25(7), 918–921 (2011).
[CrossRef] [PubMed]

Dainty, C.

de Boer, J. F.

Delori, F. C.

Dhalla, A. H.

F. LaRocca, A. H. Dhalla, M. P. Kelly, S. Farsiu, and J. A. Izatt, “Optimization of confocal scanning laser ophthalmoscope design,” J. Biomed. Opt.18(7), 076015 (2013).
[CrossRef] [PubMed]

Downes, S. M.

S. P. Hibbs, A. Smith, L. P. Chow, and S. M. Downes, “Colour photographs for screening in neovascular age-related macular degeneration: are they necessary?” Eye (Lond.)25(7), 918–921 (2011).
[CrossRef] [PubMed]

Drexler, W.

Eikelboom, R. H.

R. A. Ashman, F. Reinholz, and R. H. Eikelboom, “Improvements in Colour Fundus Imaging Using Scanning Laser Ophthalmoscopy,” Lasers Med. Sci.16(1), 52–59 (2001).
[CrossRef] [PubMed]

F. Reinholz, R. A. Ashman, and R. H. Eikelboom, “Simultaneous three wavelength imaging with a scanning laser ophthalmoscope,” Cytometry37(3), 165–170 (1999).
[CrossRef] [PubMed]

Farrow, A.

A. Manivannan, J. Van der Hoek, P. Vieira, A. Farrow, J. Olson, P. F. Sharp, and J. V. Forrester, “Clinical investigation of a true color scanning laser ophthalmoscope,” Arch. Ophthalmol.119(6), 819–824 (2001).
[CrossRef] [PubMed]

Farsiu, S.

Ferguson, R. D.

D. X. Hammer, N. V. Iftimia, T. E. Ustun, J. C. Magill, and R. D. Ferguson, “Dual OCT/SLO imager with three-dimensional tracker,” Proc. SPIE5688, 33–44 (2005).
[CrossRef]

Fernández, E. J.

Flotte, T.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Forrester, J. V.

P. Vieira, A. Manivannan, P. F. Sharp, and J. V. Forrester, “True colour imaging of the fundus using a scanning laser ophthalmoscope,” Physiol. Meas.23(1), 1–10 (2002).
[CrossRef] [PubMed]

A. Manivannan, J. Van der Hoek, P. Vieira, A. Farrow, J. Olson, P. F. Sharp, and J. V. Forrester, “Clinical investigation of a true color scanning laser ophthalmoscope,” Arch. Ophthalmol.119(6), 819–824 (2001).
[CrossRef] [PubMed]

A. Manivannan, J. N. P. Kirkpatrick, P. F. Sharp, and J. V. Forrester, “Novel approach towards colour imaging using a scanning laser ophthalmoscope,” Br. J. Ophthalmol.82(4), 342–345 (1998).
[CrossRef] [PubMed]

Freeman, W. R.

D. U. Bartsch, W. R. Freeman, and A. M. Lopez, “A false use of “true color”,” Arch. Ophthalmol.120(5), 675–676 (2002).
[PubMed]

Fujimoto, J. G.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Goncharov, A. V.

Götzinger, E.

Gregory, K.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Hammer, D. X.

D. X. Hammer, N. V. Iftimia, T. E. Ustun, J. C. Magill, and R. D. Ferguson, “Dual OCT/SLO imager with three-dimensional tracker,” Proc. SPIE5688, 33–44 (2005).
[CrossRef]

Hee, M. R.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Hermann, B.

Hibbs, S. P.

S. P. Hibbs, A. Smith, L. P. Chow, and S. M. Downes, “Colour photographs for screening in neovascular age-related macular degeneration: are they necessary?” Eye (Lond.)25(7), 918–921 (2011).
[CrossRef] [PubMed]

Hitzenberger, C. K.

Huang, D.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Hughes, G. W.

Iftimia, N. V.

D. X. Hammer, N. V. Iftimia, T. E. Ustun, J. C. Magill, and R. D. Ferguson, “Dual OCT/SLO imager with three-dimensional tracker,” Proc. SPIE5688, 33–44 (2005).
[CrossRef]

Izatt, J. A.

Jackson, D. A.

A. G. Podoleanu and D. A. Jackson, “Combined optical coherence tomograph and scanning laser ophthalmoscope,” Electron. Lett.34(11), 1088–1090 (1998).
[CrossRef]

Jaeken, B.

Jones, S. M.

Katz, M.

A. L. Lewis, M. Katz, and C. Oehrlein, “A modified achromatizing lens,” Am. J. Optom. Physiol. Opt.59(11), 909–911 (1982).
[CrossRef] [PubMed]

Kelly, M. P.

F. LaRocca, A. H. Dhalla, M. P. Kelly, S. Farsiu, and J. A. Izatt, “Optimization of confocal scanning laser ophthalmoscope design,” J. Biomed. Opt.18(7), 076015 (2013).
[CrossRef] [PubMed]

Kim, D. Y.

Kirkpatrick, J. N. P.

A. Manivannan, J. N. P. Kirkpatrick, P. F. Sharp, and J. V. Forrester, “Novel approach towards colour imaging using a scanning laser ophthalmoscope,” Br. J. Ophthalmol.82(4), 342–345 (1998).
[CrossRef] [PubMed]

LaRocca, F.

F. LaRocca, D. Nankivil, S. Farsiu, and J. A. Izatt, “Handheld simultaneous scanning laser ophthalmoscopy and optical coherence tomography system,” Biomed. Opt. Express4(11), 2307–2321 (2013).
[CrossRef] [PubMed]

F. LaRocca, A. H. Dhalla, M. P. Kelly, S. Farsiu, and J. A. Izatt, “Optimization of confocal scanning laser ophthalmoscope design,” J. Biomed. Opt.18(7), 076015 (2013).
[CrossRef] [PubMed]

Leitgeb, R. A.

Lewis, A. L.

A. L. Lewis, M. Katz, and C. Oehrlein, “A modified achromatizing lens,” Am. J. Optom. Physiol. Opt.59(11), 909–911 (1982).
[CrossRef] [PubMed]

Lin, C. P.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Lopez, A. M.

D. U. Bartsch, W. R. Freeman, and A. M. Lopez, “A false use of “true color”,” Arch. Ophthalmol.120(5), 675–676 (2002).
[PubMed]

Lott, M. N.

S. S. Ahmed, M. N. Lott, and D. M. Marcus, “The macular xanthophylls,” Surv. Ophthalmol.50(2), 183–193 (2005).
[CrossRef] [PubMed]

Lundström, L.

Magill, J. C.

D. X. Hammer, N. V. Iftimia, T. E. Ustun, J. C. Magill, and R. D. Ferguson, “Dual OCT/SLO imager with three-dimensional tracker,” Proc. SPIE5688, 33–44 (2005).
[CrossRef]

Manivannan, A.

P. Vieira, A. Manivannan, P. F. Sharp, and J. V. Forrester, “True colour imaging of the fundus using a scanning laser ophthalmoscope,” Physiol. Meas.23(1), 1–10 (2002).
[CrossRef] [PubMed]

A. Manivannan, J. Van der Hoek, P. Vieira, A. Farrow, J. Olson, P. F. Sharp, and J. V. Forrester, “Clinical investigation of a true color scanning laser ophthalmoscope,” Arch. Ophthalmol.119(6), 819–824 (2001).
[CrossRef] [PubMed]

A. Manivannan, J. N. P. Kirkpatrick, P. F. Sharp, and J. V. Forrester, “Novel approach towards colour imaging using a scanning laser ophthalmoscope,” Br. J. Ophthalmol.82(4), 342–345 (1998).
[CrossRef] [PubMed]

Manzanera, S.

Marcus, D. M.

S. S. Ahmed, M. N. Lott, and D. M. Marcus, “The macular xanthophylls,” Surv. Ophthalmol.50(2), 183–193 (2005).
[CrossRef] [PubMed]

Marques, M. J.

McLaren, K.

K. McLaren, “XIII—The Development of the CIE 1976 (L* a* b*) Uniform Colour Space and Colour-difference Formula,” J. Soc. Dyers Colourists92(9), 338–341 (1976).
[CrossRef]

Miller, D. T.

Nankivil, D.

Nielsen, M.

M. Nielsen and M. Stokes, “The Creation of the sRGB ICC Profile,” Color and Imaging Conference 1998, 253–257 (1998).

Oehrlein, C.

A. L. Lewis, M. Katz, and C. Oehrlein, “A modified achromatizing lens,” Am. J. Optom. Physiol. Opt.59(11), 909–911 (1982).
[CrossRef] [PubMed]

Olivier, S. S.

Olson, J.

A. Manivannan, J. Van der Hoek, P. Vieira, A. Farrow, J. Olson, P. F. Sharp, and J. V. Forrester, “Clinical investigation of a true color scanning laser ophthalmoscope,” Arch. Ophthalmol.119(6), 819–824 (2001).
[CrossRef] [PubMed]

Pflibsen, K. P.

Pilli, S.

Pircher, M.

Podoleanu, A. G.

Poonja, S.

Považay, B.

Powell, I.

Prieto, P. M.

Puliafito, C. A.

D. Huang, E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, C. A. Puliafito, and J. G. Fujimoto, “Optical coherence tomography,” Science254(5035), 1178–1181 (1991).
[CrossRef] [PubMed]

Reinholz, F.

R. A. Ashman, F. Reinholz, and R. H. Eikelboom, “Improvements in Colour Fundus Imaging Using Scanning Laser Ophthalmoscopy,” Lasers Med. Sci.16(1), 52–59 (2001).
[CrossRef] [PubMed]

F. Reinholz, R. A. Ashman, and R. H. Eikelboom, “Simultaneous three wavelength imaging with a scanning laser ophthalmoscope,” Cytometry37(3), 165–170 (1999).
[CrossRef] [PubMed]

Ribak, E. N.

Roorda, A.

Sattmann, H.

Schuman, J. S.

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Figures (9)

Fig. 1
Fig. 1

Side view schematic of the color SLO-OCT handheld probe design. All optical components are labeled and described in the legend. The illumination beam diameter at the eye’s pupil for SLO and OCT was 2.0 and 2.5 mm, respectively. The collection beam diameter for SLO was between 2.0 and 7.0 mm depending on the dilation of the eye’s pupil because backscattered light from the retina fills the pupil in the return path and the pupil is the limiting aperture of the SLO collection path. The collection beam diameter for OCT was the same as the OCT illumination beam diameter because the OCT illumination/collection fiber’s numerical aperture is the limiting aperture of the OCT collection path. The multimode fiber shown in the schematic is used to transfer the collected light from the SLO arm into an RGB color separation module consisting of 2 dichroic filters and 3 photomultiplier tubes (PMTs). A filter is placed in front of the red channel’s PMT to remove any contribution due to the OCT light source that is returned through the SLO collection path.

Fig. 2
Fig. 2

The SLO illumination spectrum before (A) and after (B) reshaping the visible portion of the supercontinuum laser spectrum with 2 WDMs and 3 VOAs.

Fig. 3
Fig. 3

A) Achromatizing lens (AL) design. Dimensions are given to the left of the schematic. B) Chromatic focal shift at the retina of the eye model from 400 – 900 nm after passing through all SLO optics (shown by blue line) and after correction with the AL (shown by red line). The maximum focal shift range is 950 and 7 μm for the blue and red lines, respectively.

Fig. 4
Fig. 4

Optical design spot diagrams for the illumination on the retina of a model eye spanning a 20° FOV for the “true color” SLO without (A) and with (B, C) the achromatizing lens and for the OCT system (D). The green and blue color SLO channels were warped to match the red channel in (C), to obtain an aberration-limited resolution of 7.8 μm. OCT was nearly diffraction limited at 7.5 µm. Spot diagrams are color coded for 3 wavelengths spanning the bandwidth of the respective sources and Airy disks are shown by black circles.

Fig. 5
Fig. 5

Color calibration flowchart with the raw, un-calibrated color SLO red, green, and blue (RGB) images as the input and calibrated sRGB color SLO images as the output.

Fig. 6
Fig. 6

Color calibration on color SLO and Nikon D3100 digital SLR images of a 30 patch color test target with known L*a*b* (D50) color values (A) using a least squares, polynomial calibration matrix, A ^ LS,n , described in (B). Bis a 3 × 30 matrix with the known L*a*b* (D50) values for each of the patches of the color test target. X is a (3n + 1) × 30 matrix containing the L*a*b* (D50) values of a single pixel in the color image, where n is the order of the polynomial used for fitting. “Poly1” and “poly2” correspond to first and second order polynomial fits, respectively. The mean CIE76 color differences (Mean Δ E ab * ) across all 30 patches are given for each calibration order under the images in A).

Fig. 7
Fig. 7

Imaging results from a human volunteer taken with the handheld color SLO and OCT system. A-C) 100 frame average of calibrated (2nd order polynomial) 20° FOV color SLO images taken with the focus at different depth sections with A) focused on the nerve fiber layer (NFL), B) focused on the retinal pigment epithelium (RPE), and C) focused on the choroid. D) 90 frame average of calibrated 5° FOV color SLO images at the location indicated by the dotted red square in B). The raw, un-calibrated red, green, and blue (RGB) color channels of B) are shown by E), F), and G), respectively. H) 20 frame average OCT B-scan taken at the location indicated by the dotted blue line in B). I) Image of the handheld color SLO and OCT system operated in handheld mode.

Fig. 8
Fig. 8

Color SLO imaging results taken from a human volunteer (different subject from Fig. 7). Images (100 frame averages) were taken without (A-D) and with (E-H) the achromatizing lens (AL). A) and E) are color calibrated (2nd order polynomial) color images, B) and F) are the red channel images, C) and G) are the green channel images, and D) and H) are the blue channel images. Note the reduction of the specular reflections around vessels in H) as compared to D). I) 100 frame average of calibrated 5° FOV color SLO images at the location indicated by the dotted red square in E) visualizing parafoveal cones. J) 100 frame average of calibrated 20° FOV color SLO images taken of the optic disc.

Fig. 9
Fig. 9

Comparison between two commercial multiple color SLOs and the “true color” SLO. A) Image acquired by the Optos 200 TX ultra-widefield SLO (Optos, Dunfermline, Scotland). B) Image acquired by the Spectralis HRA + OCT (6 mode) system (Heidelberg Engineering, Heidelberg, Germany). C) 100 frame average from the “true color” SLO system. The images in A) and B) have been cropped to match the field of view of the “true color” SLO.

Equations (1)

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Δ E ab * = ( L known * L meas * ) 2 + ( a known * a meas * ) 2 + ( b known * b meas * ) 2  

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