Abstract

Indocyanine green (ICG) is routinely used during surgery to stain the inner limiting membrane (ILM) and provide contrast on white light surgical microscopy. While translation of optical coherence tomography (OCT) for intraoperative imaging during ophthalmic surgery has enhanced visualization, the ILM remains difficult to distinguish from underlying retinal structures and ICG does not provide additional OCT contrast. We present photothermal OCT (PT-OCT) for high-specificity detection of ICG on retinal OCT images. We demonstrate our technique by performing an ILM peel in ex vivo eyes using low ICG concentrations and laser powers. These results establish the feasibility of PT-OCT for intraoperative guidance during retinal surgery.

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

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F. Semeraro, F. Morescalchi, S. Duse, E. Gambicorti, A. Russo, and C. Costagliola, J. Ophthalmol. 2015, 671905 (2015).
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J. M. Tucker-Schwartz, M. Lapierre-Landry, C. A. Patil, and M. C. Skala, Biomed. Opt. Express 6, 2268 (2015).
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Y. Jung, R. Reif, Y. Zeng, and R. K. Wang, Nano Lett. 11, 2938 (2011).
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S. Binder, C. I. Falkner-Radler, C. Hauger, H. Matz, and C. Glittenberg, Retina 31, 1332 (2011).
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D. C. Adler, S. W. Huang, R. Huber, and J. G. Fujimoto, Opt. Express 16, 4376 (2008).
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2005 (2)

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[Crossref]

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A. L. Oldenburg, B. E. Applegate, J. M. Tucker-Schwartz, M. C. Skala, J. Kim, and S. A. Boppart, Optical Coherence Tomography: Technology and Applications (2015), pp. 1429–1454.

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P. Saikia, T. Maisch, K. Kobuch, T. L. Jackson, W. Bäumler, R.-M. Szeimies, V.-P. Gabel, and J. Hillenkamp, Invest. Ophthalmol. Visual Sci. 47, 4998 (2006).
[Crossref]

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S. Binder, C. I. Falkner-Radler, C. Hauger, H. Matz, and C. Glittenberg, Retina 31, 1332 (2011).
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S. Pastor-Idoate, R. Bonshek, L. Irion, I. Zambrano, P. Carlin, A. Mironov, P. Bishop, D. McLeod, and P. E. Stanga, PLoS ONE 12, e0173883 (2017).
[Crossref]

Bocchio, N. L.

Bonshek, R.

S. Pastor-Idoate, R. Bonshek, L. Irion, I. Zambrano, P. Carlin, A. Mironov, P. Bishop, D. McLeod, and P. E. Stanga, PLoS ONE 12, e0173883 (2017).
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A. L. Oldenburg, B. E. Applegate, J. M. Tucker-Schwartz, M. C. Skala, J. Kim, and S. A. Boppart, Optical Coherence Tomography: Technology and Applications (2015), pp. 1429–1454.

Bouwens, A.

Carlin, P.

S. Pastor-Idoate, R. Bonshek, L. Irion, I. Zambrano, P. Carlin, A. Mironov, P. Bishop, D. McLeod, and P. E. Stanga, PLoS ONE 12, e0173883 (2017).
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Carrasco-Zevallos, O. M.

Chen, N.

B. Yuan, N. Chen, and Q. Zhu, J. Biomed. Opt. 9, 497 (2004).
[Crossref]

Choma, M. A.

Costagliola, C.

F. Semeraro, F. Morescalchi, S. Duse, E. Gambicorti, A. Russo, and C. Costagliola, J. Ophthalmol. 2015, 671905 (2015).
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Drexler, W.

Duker, J. S.

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J. P. Ehlers, J. Goshe, W. J. Dupps, P. K. Kaiser, R. P. Singh, R. Gans, J. Eisengart, and S. K. Srivastava, JAMA Ophthalmol. 133, 1124 (2015).
[Crossref]

Duse, S.

F. Semeraro, F. Morescalchi, S. Duse, E. Gambicorti, A. Russo, and C. Costagliola, J. Ophthalmol. 2015, 671905 (2015).
[Crossref]

Duvall, C.

Ehlers, J. P.

J. P. Ehlers, J. Goshe, W. J. Dupps, P. K. Kaiser, R. P. Singh, R. Gans, J. Eisengart, and S. K. Srivastava, JAMA Ophthalmol. 133, 1124 (2015).
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Y. K. Tao, J. P. Ehlers, C. A. Toth, and J. A. Izatt, Opt. Lett. 35, 3315 (2010).
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J. P. Ehlers, J. Goshe, W. J. Dupps, P. K. Kaiser, R. P. Singh, R. Gans, J. Eisengart, and S. K. Srivastava, JAMA Ophthalmol. 133, 1124 (2015).
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Falkner-Radler, C. I.

S. Binder, C. I. Falkner-Radler, C. Hauger, H. Matz, and C. Glittenberg, Retina 31, 1332 (2011).
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P. Stalmans, R. Parys-Vanginderdeuren, R. De Vos, and E. Feron, Bull. Soc. Belge Ophtalmol. 281(21), e6 (2001).

Fujimoto, J.

Fujimoto, J. G.

Gabel, V.-P.

P. Saikia, T. Maisch, K. Kobuch, T. L. Jackson, W. Bäumler, R.-M. Szeimies, V.-P. Gabel, and J. Hillenkamp, Invest. Ophthalmol. Visual Sci. 47, 4998 (2006).
[Crossref]

Gambicorti, E.

F. Semeraro, F. Morescalchi, S. Duse, E. Gambicorti, A. Russo, and C. Costagliola, J. Ophthalmol. 2015, 671905 (2015).
[Crossref]

Gandorfer, A.

A. Gandorfer, E. M. Messmer, M. W. Ulbig, and A. Kampik, Am. J. Ophthalmol. 131, 387 (2001).

Gans, R.

J. P. Ehlers, J. Goshe, W. J. Dupps, P. K. Kaiser, R. P. Singh, R. Gans, J. Eisengart, and S. K. Srivastava, JAMA Ophthalmol. 133, 1124 (2015).
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Gibson, M. I.

Glittenberg, C.

S. Binder, C. I. Falkner-Radler, C. Hauger, H. Matz, and C. Glittenberg, Retina 31, 1332 (2011).
[Crossref]

Gordon, A. Y.

M. Lapierre-Landry, A. Y. Gordon, J. S. Penn, and M. C. Skala, Sci. Rep. 7, 9228 (2017).
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Goshe, J.

J. P. Ehlers, J. Goshe, W. J. Dupps, P. K. Kaiser, R. P. Singh, R. Gans, J. Eisengart, and S. K. Srivastava, JAMA Ophthalmol. 133, 1124 (2015).
[Crossref]

Goulley, J.

Hauger, C.

S. Binder, C. I. Falkner-Radler, C. Hauger, H. Matz, and C. Glittenberg, Retina 31, 1332 (2011).
[Crossref]

Hillenkamp, J.

P. Saikia, T. Maisch, K. Kobuch, T. L. Jackson, W. Bäumler, R.-M. Szeimies, V.-P. Gabel, and J. Hillenkamp, Invest. Ophthalmol. Visual Sci. 47, 4998 (2006).
[Crossref]

Horiuchi, S.

M. Murata, S. Shimizu, S. Horiuchi, and S. Sato, Retina 25, 75 (2005).
[Crossref]

Hu, C.

C. Hu, F. E. Muller-Karger, and R. G. Zepp, Limnol. Oceanogr. 47, 1261 (2002).
[Crossref]

Huang, S. W.

Huber, R.

Ippen, E.

Irion, L.

S. Pastor-Idoate, R. Bonshek, L. Irion, I. Zambrano, P. Carlin, A. Mironov, P. Bishop, D. McLeod, and P. E. Stanga, PLoS ONE 12, e0173883 (2017).
[Crossref]

Izatt, J. A.

Jackson, T. L.

P. Saikia, T. Maisch, K. Kobuch, T. L. Jackson, W. Bäumler, R.-M. Szeimies, V.-P. Gabel, and J. Hillenkamp, Invest. Ophthalmol. Visual Sci. 47, 4998 (2006).
[Crossref]

Jung, Y.

Y. Jung, R. Reif, Y. Zeng, and R. K. Wang, Nano Lett. 11, 2938 (2011).
[Crossref]

Kaiser, P. K.

J. P. Ehlers, J. Goshe, W. J. Dupps, P. K. Kaiser, R. P. Singh, R. Gans, J. Eisengart, and S. K. Srivastava, JAMA Ophthalmol. 133, 1124 (2015).
[Crossref]

Kampik, A.

A. Gandorfer, E. M. Messmer, M. W. Ulbig, and A. Kampik, Am. J. Ophthalmol. 131, 387 (2001).

Kärtner, F.

Keller, B.

Kim, J.

A. L. Oldenburg, B. E. Applegate, J. M. Tucker-Schwartz, M. C. Skala, J. Kim, and S. A. Boppart, Optical Coherence Tomography: Technology and Applications (2015), pp. 1429–1454.

Ko, T. H.

Kobuch, K.

P. Saikia, T. Maisch, K. Kobuch, T. L. Jackson, W. Bäumler, R.-M. Szeimies, V.-P. Gabel, and J. Hillenkamp, Invest. Ophthalmol. Visual Sci. 47, 4998 (2006).
[Crossref]

Kowalczyk, A.

Kuo, A. N.

Kwant, G.

M. Landsman, G. Kwant, G. Mook, and W. Zijlstra, J. Appl. Physiol. 40, 575 (1976).
[Crossref]

Kwok, A. K.

A. K. Kwok, T. Y. Lai, D. T. Yew, and W. W. Li, Am. J. Ophthalmol. 136, 223 (2003).

Lai, T. Y.

A. K. Kwok, T. Y. Lai, D. T. Yew, and W. W. Li, Am. J. Ophthalmol. 136, 223 (2003).

Landsman, M.

M. Landsman, G. Kwant, G. Mook, and W. Zijlstra, J. Appl. Physiol. 40, 575 (1976).
[Crossref]

Lapierre-Landry, M.

M. Lapierre-Landry, A. Y. Gordon, J. S. Penn, and M. C. Skala, Sci. Rep. 7, 9228 (2017).
[Crossref]

M. Lapierre-Landry, J. M. Tucker-Schwartz, and M. C. Skala, Biomedical Opt. Express 7, 2607 (2016).
[Crossref]

J. M. Tucker-Schwartz, M. Lapierre-Landry, C. A. Patil, and M. C. Skala, Biomed. Opt. Express 6, 2268 (2015).
[Crossref]

Lasser, T.

Li, W. W.

A. K. Kwok, T. Y. Lai, D. T. Yew, and W. W. Li, Am. J. Ophthalmol. 136, 223 (2003).

Li, X.

Maisch, T.

P. Saikia, T. Maisch, K. Kobuch, T. L. Jackson, W. Bäumler, R.-M. Szeimies, V.-P. Gabel, and J. Hillenkamp, Invest. Ophthalmol. Visual Sci. 47, 4998 (2006).
[Crossref]

Matz, H.

S. Binder, C. I. Falkner-Radler, C. Hauger, H. Matz, and C. Glittenberg, Retina 31, 1332 (2011).
[Crossref]

McCarty, O. J.

McLeod, D.

S. Pastor-Idoate, R. Bonshek, L. Irion, I. Zambrano, P. Carlin, A. Mironov, P. Bishop, D. McLeod, and P. E. Stanga, PLoS ONE 12, e0173883 (2017).
[Crossref]

Messmer, E. M.

A. Gandorfer, E. M. Messmer, M. W. Ulbig, and A. Kampik, Am. J. Ophthalmol. 131, 387 (2001).

Meyer, T.

Mironov, A.

S. Pastor-Idoate, R. Bonshek, L. Irion, I. Zambrano, P. Carlin, A. Mironov, P. Bishop, D. McLeod, and P. E. Stanga, PLoS ONE 12, e0173883 (2017).
[Crossref]

Mook, G.

M. Landsman, G. Kwant, G. Mook, and W. Zijlstra, J. Appl. Physiol. 40, 575 (1976).
[Crossref]

Morescalchi, F.

F. Semeraro, F. Morescalchi, S. Duse, E. Gambicorti, A. Russo, and C. Costagliola, J. Ophthalmol. 2015, 671905 (2015).
[Crossref]

Morgner, U.

Muller-Karger, F. E.

C. Hu, F. E. Muller-Karger, and R. G. Zepp, Limnol. Oceanogr. 47, 1261 (2002).
[Crossref]

Murata, M.

M. Murata, S. Shimizu, S. Horiuchi, and S. Sato, Retina 25, 75 (2005).
[Crossref]

Oldenburg, A. L.

A. L. Oldenburg, F. J.-J. Toublan, K. S. Suslick, A. Wei, and S. A. Boppart, Opt. Express 13, 6597 (2005).
[Crossref]

A. L. Oldenburg, B. E. Applegate, J. M. Tucker-Schwartz, M. C. Skala, J. Kim, and S. A. Boppart, Optical Coherence Tomography: Technology and Applications (2015), pp. 1429–1454.

Pache, C.

Parys-Vanginderdeuren, R.

P. Stalmans, R. Parys-Vanginderdeuren, R. De Vos, and E. Feron, Bull. Soc. Belge Ophtalmol. 281(21), e6 (2001).

Pastor-Idoate, S.

S. Pastor-Idoate, R. Bonshek, L. Irion, I. Zambrano, P. Carlin, A. Mironov, P. Bishop, D. McLeod, and P. E. Stanga, PLoS ONE 12, e0173883 (2017).
[Crossref]

Patil, C.

Patil, C. A.

Penn, J. S.

M. Lapierre-Landry, A. Y. Gordon, J. S. Penn, and M. C. Skala, Sci. Rep. 7, 9228 (2017).
[Crossref]

Pitris, C.

Rao, K. D.

Reif, R.

Y. Jung, R. Reif, Y. Zeng, and R. K. Wang, Nano Lett. 11, 2938 (2011).
[Crossref]

Rollins, A. M.

Russo, A.

F. Semeraro, F. Morescalchi, S. Duse, E. Gambicorti, A. Russo, and C. Costagliola, J. Ophthalmol. 2015, 671905 (2015).
[Crossref]

Saikia, P.

P. Saikia, T. Maisch, K. Kobuch, T. L. Jackson, W. Bäumler, R.-M. Szeimies, V.-P. Gabel, and J. Hillenkamp, Invest. Ophthalmol. Visual Sci. 47, 4998 (2006).
[Crossref]

Santschi, C.

Sato, S.

M. Murata, S. Shimizu, S. Horiuchi, and S. Sato, Retina 25, 75 (2005).
[Crossref]

Semeraro, F.

F. Semeraro, F. Morescalchi, S. Duse, E. Gambicorti, A. Russo, and C. Costagliola, J. Ophthalmol. 2015, 671905 (2015).
[Crossref]

Shimizu, S.

M. Murata, S. Shimizu, S. Horiuchi, and S. Sato, Retina 25, 75 (2005).
[Crossref]

Singh, R. P.

J. P. Ehlers, J. Goshe, W. J. Dupps, P. K. Kaiser, R. P. Singh, R. Gans, J. Eisengart, and S. K. Srivastava, JAMA Ophthalmol. 133, 1124 (2015).
[Crossref]

Skala, M.

Skala, M. C.

M. Lapierre-Landry, A. Y. Gordon, J. S. Penn, and M. C. Skala, Sci. Rep. 7, 9228 (2017).
[Crossref]

M. Lapierre-Landry, J. M. Tucker-Schwartz, and M. C. Skala, Biomedical Opt. Express 7, 2607 (2016).
[Crossref]

J. M. Tucker-Schwartz, M. Lapierre-Landry, C. A. Patil, and M. C. Skala, Biomed. Opt. Express 6, 2268 (2015).
[Crossref]

M. C. Skala, M. J. Crow, A. Wax, and J. A. Izatt, Nano Lett. 8, 3461 (2008).
[Crossref]

A. L. Oldenburg, B. E. Applegate, J. M. Tucker-Schwartz, M. C. Skala, J. Kim, and S. A. Boppart, Optical Coherence Tomography: Technology and Applications (2015), pp. 1429–1454.

Smith, J. W.

Srinivasan, V. J.

Srivastava, S. K.

J. P. Ehlers, J. Goshe, W. J. Dupps, P. K. Kaiser, R. P. Singh, R. Gans, J. Eisengart, and S. K. Srivastava, JAMA Ophthalmol. 133, 1124 (2015).
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Biomed. Opt. Express (3)

Biomedical Opt. Express (1)

M. Lapierre-Landry, J. M. Tucker-Schwartz, and M. C. Skala, Biomedical Opt. Express 7, 2607 (2016).
[Crossref]

Biostat. Anal. (1)

J. H. Zar, Biostat. Anal. 2, 292 (1984).

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P. Stalmans, R. Parys-Vanginderdeuren, R. De Vos, and E. Feron, Bull. Soc. Belge Ophtalmol. 281(21), e6 (2001).

Invest. Ophthalmol. Visual Sci. (1)

P. Saikia, T. Maisch, K. Kobuch, T. L. Jackson, W. Bäumler, R.-M. Szeimies, V.-P. Gabel, and J. Hillenkamp, Invest. Ophthalmol. Visual Sci. 47, 4998 (2006).
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J. Appl. Physiol. (1)

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J. Biomed. Opt. (1)

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JAMA Ophthalmol. (1)

J. P. Ehlers, J. Goshe, W. J. Dupps, P. K. Kaiser, R. P. Singh, R. Gans, J. Eisengart, and S. K. Srivastava, JAMA Ophthalmol. 133, 1124 (2015).
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C. Hu, F. E. Muller-Karger, and R. G. Zepp, Limnol. Oceanogr. 47, 1261 (2002).
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Opt. Express (4)

Opt. Lett. (4)

PLoS ONE (1)

S. Pastor-Idoate, R. Bonshek, L. Irion, I. Zambrano, P. Carlin, A. Mironov, P. Bishop, D. McLeod, and P. E. Stanga, PLoS ONE 12, e0173883 (2017).
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M. Lapierre-Landry, A. Y. Gordon, J. S. Penn, and M. C. Skala, Sci. Rep. 7, 9228 (2017).
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Other (2)

American National Standards Institute, Safe Use of Lasers (ANSI/UL) (2014).

A. L. Oldenburg, B. E. Applegate, J. M. Tucker-Schwartz, M. C. Skala, J. Kim, and S. A. Boppart, Optical Coherence Tomography: Technology and Applications (2015), pp. 1429–1454.

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Figures (3)

Fig. 1.
Fig. 1. (a) Average PT-OCT signal as a function of photothermal laser power for all ICG phantom concentrations. Dashed lines: linear fit for low concentration samples. Error bar: standard deviation over one B-scan. (b) PT-OCT signal for 0.16 mg/cc of ICG (orange) in comparison to saline (blue) as a function of laser power. (c) PT-OCT signal as a function of ICG concentration using 0.48 mW (orange) or 0 mW (blue) of laser power. Linear fit (solid lines), with 95% confidence interval (dotted lines). p < 0.05 * , p < 0.001 * * * * difference between slopes.
Fig. 2.
Fig. 2. PT-OCT of an ex vivo porcine retina after the ILM was stained with 0.5 mg/cc of ICG. (a) OCT (gray) and (b) corresponding PT-OCT B-scans (overlaid in green) using 0.89 mW or (c) 3.12 mW of photothermal laser power. Magnified view of the boxed area in (d) and (e). Scale bar: 200 μm.
Fig. 3.
Fig. 3. PT-OCT of an ILM-peel in ex vivo pig eye. (a) White light image from the surgical microscope showing the boundary between the intact ILM dyed with 0.25 mg/cc ICG and the peeled ILM (arrows) with the B-scan location (dashed line). (b) OCT (gray) and (c) corresponding PT-OCT B-scan (green) showing a cross-section of the retina with intact ILM and after it was peeled (arrows at boundary). (d) Magnified view of boxed area in (c). Scale bar: 200 μm.

Equations (2)

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PTOCT Δ T = P 0 μ a 4 α π ρ c ln ( 1 + t L α w ( z ) 2 / 8 ) ,
PTOCT ( z ) = | p ( z , f 0 ) | λ 4 π 2 f 0 n Δ t ,