Abstract

We report on the wavelength dependence of second harmonic generation (SHG) of collagen in scattering tissues over the wavelength range of 800–1200 nm. The study incorporates inclusion of the molecular hyperpolarizability β of collagen and optical scattering, both of which are wavelength dependent. Using 3D SHG imaging and Monte Carlo simulations, we find the wavelength dependence of β is not well described by a two-state model based on known absorption bands. We further find that longer wavelength excitation is inefficient as the reduction in scattering is overcome by the decreased β far from resonance and the optimal excitation is within the 800–900 nm range. The impact is larger for backward collected SHG.

© 2014 Optical Society of America

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  1. P. J. Campagnola and C. Y. Dong, Laser Photon. Rev. 5, 13 (2011).
    [CrossRef]
  2. P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, BMC Med. 6, 11 (2008).
    [CrossRef]
  3. O. Nadiarnykh, R. B. Lacomb, M. A. Brewer, and P. J. Campagnola, BMC Cancer 10, 94 (2010).
    [CrossRef]
  4. M. Strupler, A. M. Pena, M. Hernest, P. L. Tharaux, J. L. Martin, E. Beaurepaire, and M. C. Schanne-Klein, Opt. Express 15, 4054 (2007).
    [CrossRef]
  5. R. Lacomb, O. Nadiarnykh, and P. J. Campagnola, Biophys. J. 94, 4504 (2008).
    [CrossRef]
  6. R. Lacomb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, Opt. Commun. 281, 1823 (2008).
    [CrossRef]
  7. J. Mertz and L. Moreaux, Opt. Commun. 196, 325 (2001).
    [CrossRef]
  8. J. L. Oudar and D. S. Chemla, J. Chem. Phys. 66, 2664 (1977).
    [CrossRef]
  9. R. Richards-Kortum and E. Sevick-Muraca, Annu. Rev. Phys. Chem. 47, 555 (1996).
    [CrossRef]
  10. T. A. Theodossiou, C. Thrasivoulou, C. Ekwobi, and D. L. Becker, Biophys. J. 91, 4665 (2006).
    [CrossRef]
  11. W. R. Zipfel, R. M. Williams, and W. W. Webb, Nat. Biotechnol. 21, 1369 (2003).
    [CrossRef]
  12. A. Zoumi, A. Yeh, and B. J. Tromberg, Proc. Natl. Acad. Sci. USA 99, 11014 (2002).
    [CrossRef]
  13. M. Shen, J. Zhao, H. Zeng, and S. Tang, J. Biomed. Opt. 18, 031109 (2013).
    [CrossRef]
  14. X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, Nat. Protocols 7, 654 (2012).
    [CrossRef]
  15. G. Hall, K. W. Eliceiri, and P. J. Campagnola, J. Biomed. Opt. 18, 116008 (2013).
    [CrossRef]
  16. G. Hall, S. L. Jacques, K. W. Eliceiri, and P. J. Campagnola, Biomed. Opt. Express 3, 2707 (2012).
    [CrossRef]
  17. J. W. Caldwell and J. Applequist, Biopolymers 23, 1891 (1984).
    [CrossRef]
  18. O. Nadiarnykh and P. J. Campagnola, Opt. Express 17, 5794 (2009).
    [CrossRef]

2013 (2)

M. Shen, J. Zhao, H. Zeng, and S. Tang, J. Biomed. Opt. 18, 031109 (2013).
[CrossRef]

G. Hall, K. W. Eliceiri, and P. J. Campagnola, J. Biomed. Opt. 18, 116008 (2013).
[CrossRef]

2012 (2)

G. Hall, S. L. Jacques, K. W. Eliceiri, and P. J. Campagnola, Biomed. Opt. Express 3, 2707 (2012).
[CrossRef]

X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, Nat. Protocols 7, 654 (2012).
[CrossRef]

2011 (1)

P. J. Campagnola and C. Y. Dong, Laser Photon. Rev. 5, 13 (2011).
[CrossRef]

2010 (1)

O. Nadiarnykh, R. B. Lacomb, M. A. Brewer, and P. J. Campagnola, BMC Cancer 10, 94 (2010).
[CrossRef]

2009 (1)

2008 (3)

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, BMC Med. 6, 11 (2008).
[CrossRef]

R. Lacomb, O. Nadiarnykh, and P. J. Campagnola, Biophys. J. 94, 4504 (2008).
[CrossRef]

R. Lacomb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, Opt. Commun. 281, 1823 (2008).
[CrossRef]

2007 (1)

2006 (1)

T. A. Theodossiou, C. Thrasivoulou, C. Ekwobi, and D. L. Becker, Biophys. J. 91, 4665 (2006).
[CrossRef]

2003 (1)

W. R. Zipfel, R. M. Williams, and W. W. Webb, Nat. Biotechnol. 21, 1369 (2003).
[CrossRef]

2002 (1)

A. Zoumi, A. Yeh, and B. J. Tromberg, Proc. Natl. Acad. Sci. USA 99, 11014 (2002).
[CrossRef]

2001 (1)

J. Mertz and L. Moreaux, Opt. Commun. 196, 325 (2001).
[CrossRef]

1996 (1)

R. Richards-Kortum and E. Sevick-Muraca, Annu. Rev. Phys. Chem. 47, 555 (1996).
[CrossRef]

1984 (1)

J. W. Caldwell and J. Applequist, Biopolymers 23, 1891 (1984).
[CrossRef]

1977 (1)

J. L. Oudar and D. S. Chemla, J. Chem. Phys. 66, 2664 (1977).
[CrossRef]

Applequist, J.

J. W. Caldwell and J. Applequist, Biopolymers 23, 1891 (1984).
[CrossRef]

Beaurepaire, E.

Becker, D. L.

T. A. Theodossiou, C. Thrasivoulou, C. Ekwobi, and D. L. Becker, Biophys. J. 91, 4665 (2006).
[CrossRef]

Brewer, M. A.

O. Nadiarnykh, R. B. Lacomb, M. A. Brewer, and P. J. Campagnola, BMC Cancer 10, 94 (2010).
[CrossRef]

Caldwell, J. W.

J. W. Caldwell and J. Applequist, Biopolymers 23, 1891 (1984).
[CrossRef]

Campagnola, P. J.

G. Hall, K. W. Eliceiri, and P. J. Campagnola, J. Biomed. Opt. 18, 116008 (2013).
[CrossRef]

G. Hall, S. L. Jacques, K. W. Eliceiri, and P. J. Campagnola, Biomed. Opt. Express 3, 2707 (2012).
[CrossRef]

X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, Nat. Protocols 7, 654 (2012).
[CrossRef]

P. J. Campagnola and C. Y. Dong, Laser Photon. Rev. 5, 13 (2011).
[CrossRef]

O. Nadiarnykh, R. B. Lacomb, M. A. Brewer, and P. J. Campagnola, BMC Cancer 10, 94 (2010).
[CrossRef]

O. Nadiarnykh and P. J. Campagnola, Opt. Express 17, 5794 (2009).
[CrossRef]

R. Lacomb, O. Nadiarnykh, and P. J. Campagnola, Biophys. J. 94, 4504 (2008).
[CrossRef]

R. Lacomb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, Opt. Commun. 281, 1823 (2008).
[CrossRef]

Chemla, D. S.

J. L. Oudar and D. S. Chemla, J. Chem. Phys. 66, 2664 (1977).
[CrossRef]

Chen, X.

X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, Nat. Protocols 7, 654 (2012).
[CrossRef]

Dong, C. Y.

P. J. Campagnola and C. Y. Dong, Laser Photon. Rev. 5, 13 (2011).
[CrossRef]

Ekwobi, C.

T. A. Theodossiou, C. Thrasivoulou, C. Ekwobi, and D. L. Becker, Biophys. J. 91, 4665 (2006).
[CrossRef]

Eliceiri, K. W.

G. Hall, K. W. Eliceiri, and P. J. Campagnola, J. Biomed. Opt. 18, 116008 (2013).
[CrossRef]

G. Hall, S. L. Jacques, K. W. Eliceiri, and P. J. Campagnola, Biomed. Opt. Express 3, 2707 (2012).
[CrossRef]

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, BMC Med. 6, 11 (2008).
[CrossRef]

Hall, G.

G. Hall, K. W. Eliceiri, and P. J. Campagnola, J. Biomed. Opt. 18, 116008 (2013).
[CrossRef]

G. Hall, S. L. Jacques, K. W. Eliceiri, and P. J. Campagnola, Biomed. Opt. Express 3, 2707 (2012).
[CrossRef]

Hernest, M.

Inman, D. R.

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, BMC Med. 6, 11 (2008).
[CrossRef]

Jacques, S. L.

Keely, P. J.

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, BMC Med. 6, 11 (2008).
[CrossRef]

Knittel, J. G.

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, BMC Med. 6, 11 (2008).
[CrossRef]

Lacomb, R.

R. Lacomb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, Opt. Commun. 281, 1823 (2008).
[CrossRef]

R. Lacomb, O. Nadiarnykh, and P. J. Campagnola, Biophys. J. 94, 4504 (2008).
[CrossRef]

Lacomb, R. B.

O. Nadiarnykh, R. B. Lacomb, M. A. Brewer, and P. J. Campagnola, BMC Cancer 10, 94 (2010).
[CrossRef]

Martin, J. L.

Mertz, J.

J. Mertz and L. Moreaux, Opt. Commun. 196, 325 (2001).
[CrossRef]

Moreaux, L.

J. Mertz and L. Moreaux, Opt. Commun. 196, 325 (2001).
[CrossRef]

Nadiarnykh, O.

O. Nadiarnykh, R. B. Lacomb, M. A. Brewer, and P. J. Campagnola, BMC Cancer 10, 94 (2010).
[CrossRef]

O. Nadiarnykh and P. J. Campagnola, Opt. Express 17, 5794 (2009).
[CrossRef]

R. Lacomb, O. Nadiarnykh, and P. J. Campagnola, Biophys. J. 94, 4504 (2008).
[CrossRef]

R. Lacomb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, Opt. Commun. 281, 1823 (2008).
[CrossRef]

Nadiarynkh, O.

X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, Nat. Protocols 7, 654 (2012).
[CrossRef]

Oudar, J. L.

J. L. Oudar and D. S. Chemla, J. Chem. Phys. 66, 2664 (1977).
[CrossRef]

Pena, A. M.

Plotnikov, S.

X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, Nat. Protocols 7, 654 (2012).
[CrossRef]

Provenzano, P. P.

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, BMC Med. 6, 11 (2008).
[CrossRef]

Richards-Kortum, R.

R. Richards-Kortum and E. Sevick-Muraca, Annu. Rev. Phys. Chem. 47, 555 (1996).
[CrossRef]

Rueden, C. T.

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, BMC Med. 6, 11 (2008).
[CrossRef]

Schanne-Klein, M. C.

Sevick-Muraca, E.

R. Richards-Kortum and E. Sevick-Muraca, Annu. Rev. Phys. Chem. 47, 555 (1996).
[CrossRef]

Shen, M.

M. Shen, J. Zhao, H. Zeng, and S. Tang, J. Biomed. Opt. 18, 031109 (2013).
[CrossRef]

Strupler, M.

Tang, S.

M. Shen, J. Zhao, H. Zeng, and S. Tang, J. Biomed. Opt. 18, 031109 (2013).
[CrossRef]

Tharaux, P. L.

Theodossiou, T. A.

T. A. Theodossiou, C. Thrasivoulou, C. Ekwobi, and D. L. Becker, Biophys. J. 91, 4665 (2006).
[CrossRef]

Thrasivoulou, C.

T. A. Theodossiou, C. Thrasivoulou, C. Ekwobi, and D. L. Becker, Biophys. J. 91, 4665 (2006).
[CrossRef]

Townsend, S. S.

R. Lacomb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, Opt. Commun. 281, 1823 (2008).
[CrossRef]

Tromberg, B. J.

A. Zoumi, A. Yeh, and B. J. Tromberg, Proc. Natl. Acad. Sci. USA 99, 11014 (2002).
[CrossRef]

Webb, W. W.

W. R. Zipfel, R. M. Williams, and W. W. Webb, Nat. Biotechnol. 21, 1369 (2003).
[CrossRef]

White, J. G.

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, BMC Med. 6, 11 (2008).
[CrossRef]

Williams, R. M.

W. R. Zipfel, R. M. Williams, and W. W. Webb, Nat. Biotechnol. 21, 1369 (2003).
[CrossRef]

Yan, L.

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, BMC Med. 6, 11 (2008).
[CrossRef]

Yeh, A.

A. Zoumi, A. Yeh, and B. J. Tromberg, Proc. Natl. Acad. Sci. USA 99, 11014 (2002).
[CrossRef]

Zeng, H.

M. Shen, J. Zhao, H. Zeng, and S. Tang, J. Biomed. Opt. 18, 031109 (2013).
[CrossRef]

Zhao, J.

M. Shen, J. Zhao, H. Zeng, and S. Tang, J. Biomed. Opt. 18, 031109 (2013).
[CrossRef]

Zipfel, W. R.

W. R. Zipfel, R. M. Williams, and W. W. Webb, Nat. Biotechnol. 21, 1369 (2003).
[CrossRef]

Zoumi, A.

A. Zoumi, A. Yeh, and B. J. Tromberg, Proc. Natl. Acad. Sci. USA 99, 11014 (2002).
[CrossRef]

Annu. Rev. Phys. Chem. (1)

R. Richards-Kortum and E. Sevick-Muraca, Annu. Rev. Phys. Chem. 47, 555 (1996).
[CrossRef]

Biomed. Opt. Express (1)

Biophys. J. (2)

R. Lacomb, O. Nadiarnykh, and P. J. Campagnola, Biophys. J. 94, 4504 (2008).
[CrossRef]

T. A. Theodossiou, C. Thrasivoulou, C. Ekwobi, and D. L. Becker, Biophys. J. 91, 4665 (2006).
[CrossRef]

Biopolymers (1)

J. W. Caldwell and J. Applequist, Biopolymers 23, 1891 (1984).
[CrossRef]

BMC Cancer (1)

O. Nadiarnykh, R. B. Lacomb, M. A. Brewer, and P. J. Campagnola, BMC Cancer 10, 94 (2010).
[CrossRef]

BMC Med. (1)

P. P. Provenzano, D. R. Inman, K. W. Eliceiri, J. G. Knittel, L. Yan, C. T. Rueden, J. G. White, and P. J. Keely, BMC Med. 6, 11 (2008).
[CrossRef]

J. Biomed. Opt. (2)

G. Hall, K. W. Eliceiri, and P. J. Campagnola, J. Biomed. Opt. 18, 116008 (2013).
[CrossRef]

M. Shen, J. Zhao, H. Zeng, and S. Tang, J. Biomed. Opt. 18, 031109 (2013).
[CrossRef]

J. Chem. Phys. (1)

J. L. Oudar and D. S. Chemla, J. Chem. Phys. 66, 2664 (1977).
[CrossRef]

Laser Photon. Rev. (1)

P. J. Campagnola and C. Y. Dong, Laser Photon. Rev. 5, 13 (2011).
[CrossRef]

Nat. Biotechnol. (1)

W. R. Zipfel, R. M. Williams, and W. W. Webb, Nat. Biotechnol. 21, 1369 (2003).
[CrossRef]

Nat. Protocols (1)

X. Chen, O. Nadiarynkh, S. Plotnikov, and P. J. Campagnola, Nat. Protocols 7, 654 (2012).
[CrossRef]

Opt. Commun. (2)

R. Lacomb, O. Nadiarnykh, S. S. Townsend, and P. J. Campagnola, Opt. Commun. 281, 1823 (2008).
[CrossRef]

J. Mertz and L. Moreaux, Opt. Commun. 196, 325 (2001).
[CrossRef]

Opt. Express (2)

Proc. Natl. Acad. Sci. USA (1)

A. Zoumi, A. Yeh, and B. J. Tromberg, Proc. Natl. Acad. Sci. USA 99, 11014 (2002).
[CrossRef]

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Figures (4)

Fig. 1.
Fig. 1.

Representative forward SHG depth response in tendon over a wide wavelength range. Each curve has been accounted for excitation power, pulse width, and PMT detector sensitivity. Error bars represent the standard error of the mean for measurements at three locations of similar thickness.

Fig. 2.
Fig. 2.

SHG strength of tendon as function of wavelength based on a two-state model for comparison.

Fig. 3.
Fig. 3.

Simulation of signal attenuation in ovarian tissue. The forward and backward signals are shown with solid and open circles, respectively.

Fig. 4.
Fig. 4.

SHG wavelength-dependent experimental attenuation curves for adenocarcinoma of human ovary.

Tables (1)

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Table 1. Measured Optical Properties of Tissues

Equations (1)

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deff2β2=(3e22mω0fΔμ(ω02ω12)(ω02ω22))2,

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