Abstract

We present a hybrid microscope combining multiphoton microscopy incorporating second-harmonic generation contrast and optical-resolution optoacoustic (photoacoustic) microscopy. We study the relative performance of the two systems and investigate the complementarity of contrast by demonstrating the label-free imaging capabilities of the hybrid microscope on zebrafish larvae ex vivo, concurrently visualizing the fish musculature and melanocytes. This implementation can prove useful in multiparametric microscopy studies, enabling broader information to be collected from biological specimens.

© 2014 Optical Society of America

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  1. R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, J. Biomed. Opt. 6, 129 (2013).
  2. P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, Biophys. J. 82, 493 (2002).
    [CrossRef]
  3. S. Psilodimitrakopoulos, V. Petegnief, G. Soria, I. Amat-Roldan, D. Artigas, A. Planas, and P. Loza-Alvarez, Opt. Express 17, 14418 (2009).
    [CrossRef]
  4. N. Mazumder, J. Qiu, M. Foreman, C. Romero, P. Török, and F. Kao, Biomed. Opt. Express 4, 538 (2013).
    [CrossRef]
  5. S. Psilodimitrakopoulos, V. Petegnief, N. De Vera, O. Hernandez, D. Artigas, A. M. Planas, and P. Loza-Alvarez, Biophys. J. 104, 968 (2013).
    [CrossRef]
  6. G. J. Tserevelakis, E. V. Megalou, G. Filippidis, B. Petanidou, C. Fotakis, and N. Tavernarakis, PLoS ONE 9, e84431 (2014).
    [CrossRef]
  7. C. Vinegoni, T. Ralston, W. Tan, W. Luo, D. L. Marks, and S. A. Boppart, Appl. Phys. Lett. 88, 053901 (2006).
    [CrossRef]
  8. V. Ntziachristos, Nat. Methods 7, 603 (2010).
    [CrossRef]
  9. Y. Wang, S. Hu, K. Maslov, Y. Zhang, Y. Xia, and L. V. Wang, Opt. Lett. 36, 1029 (2011).
    [CrossRef]
  10. S. Jiao, Z. Xie, H. F. Zhang, and C. A. Puliafito, Opt. Lett. 34, 2961 (2009).
    [CrossRef]
  11. H. F. Zhang, J. Wang, Q. Wei, T. Liu, S. Jiao, and C. A. Puliafito, Opt. Express 18, 1278 (2010).
    [CrossRef]
  12. X. Zhang, H. F. Zhang, C. A. Puliafito, and S. Jiao, J. Biomed. Opt. 16, 080504 (2011).
    [CrossRef]
  13. G. Langer, K. D. Bouchal, H. Grün, P. Burgholzer, and T. Berer, Opt. Express 21, 22410 (2013).
    [CrossRef]
  14. R. Ma, S. Söntges, S. Shoham, V. Ntziachristos, and D. Razansky, Biomed. Opt. Express 3, 1724 (2012).
    [CrossRef]
  15. M. Omar, J. Gateau, and V. Ntziachristos, Opt. Lett. 38, 2472 (2013).
    [CrossRef]
  16. D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, and V. Ntziachristos, Nat. Photonics 3, 412 (2009).
    [CrossRef]

2014 (1)

G. J. Tserevelakis, E. V. Megalou, G. Filippidis, B. Petanidou, C. Fotakis, and N. Tavernarakis, PLoS ONE 9, e84431 (2014).
[CrossRef]

2013 (5)

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, J. Biomed. Opt. 6, 129 (2013).

N. Mazumder, J. Qiu, M. Foreman, C. Romero, P. Török, and F. Kao, Biomed. Opt. Express 4, 538 (2013).
[CrossRef]

S. Psilodimitrakopoulos, V. Petegnief, N. De Vera, O. Hernandez, D. Artigas, A. M. Planas, and P. Loza-Alvarez, Biophys. J. 104, 968 (2013).
[CrossRef]

G. Langer, K. D. Bouchal, H. Grün, P. Burgholzer, and T. Berer, Opt. Express 21, 22410 (2013).
[CrossRef]

M. Omar, J. Gateau, and V. Ntziachristos, Opt. Lett. 38, 2472 (2013).
[CrossRef]

2012 (1)

2011 (2)

Y. Wang, S. Hu, K. Maslov, Y. Zhang, Y. Xia, and L. V. Wang, Opt. Lett. 36, 1029 (2011).
[CrossRef]

X. Zhang, H. F. Zhang, C. A. Puliafito, and S. Jiao, J. Biomed. Opt. 16, 080504 (2011).
[CrossRef]

2010 (2)

2009 (3)

2006 (1)

C. Vinegoni, T. Ralston, W. Tan, W. Luo, D. L. Marks, and S. A. Boppart, Appl. Phys. Lett. 88, 053901 (2006).
[CrossRef]

2002 (1)

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, Biophys. J. 82, 493 (2002).
[CrossRef]

Amat-Roldan, I.

Artigas, D.

S. Psilodimitrakopoulos, V. Petegnief, N. De Vera, O. Hernandez, D. Artigas, A. M. Planas, and P. Loza-Alvarez, Biophys. J. 104, 968 (2013).
[CrossRef]

S. Psilodimitrakopoulos, V. Petegnief, G. Soria, I. Amat-Roldan, D. Artigas, A. Planas, and P. Loza-Alvarez, Opt. Express 17, 14418 (2009).
[CrossRef]

Berer, T.

Boppart, S. A.

C. Vinegoni, T. Ralston, W. Tan, W. Luo, D. L. Marks, and S. A. Boppart, Appl. Phys. Lett. 88, 053901 (2006).
[CrossRef]

Bouchal, K. D.

Burgholzer, P.

Campagnola, P. J.

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, Biophys. J. 82, 493 (2002).
[CrossRef]

Cicchi, R.

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, J. Biomed. Opt. 6, 129 (2013).

De Vera, N.

S. Psilodimitrakopoulos, V. Petegnief, N. De Vera, O. Hernandez, D. Artigas, A. M. Planas, and P. Loza-Alvarez, Biophys. J. 104, 968 (2013).
[CrossRef]

Dietzek, B.

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, J. Biomed. Opt. 6, 129 (2013).

Distel, M.

D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, and V. Ntziachristos, Nat. Photonics 3, 412 (2009).
[CrossRef]

Filippidis, G.

G. J. Tserevelakis, E. V. Megalou, G. Filippidis, B. Petanidou, C. Fotakis, and N. Tavernarakis, PLoS ONE 9, e84431 (2014).
[CrossRef]

Foreman, M.

Fotakis, C.

G. J. Tserevelakis, E. V. Megalou, G. Filippidis, B. Petanidou, C. Fotakis, and N. Tavernarakis, PLoS ONE 9, e84431 (2014).
[CrossRef]

Gateau, J.

Grün, H.

Hernandez, O.

S. Psilodimitrakopoulos, V. Petegnief, N. De Vera, O. Hernandez, D. Artigas, A. M. Planas, and P. Loza-Alvarez, Biophys. J. 104, 968 (2013).
[CrossRef]

Hoppe, P. E.

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, Biophys. J. 82, 493 (2002).
[CrossRef]

Hu, S.

Jiao, S.

Kao, F.

Kapsokalyvas, D.

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, J. Biomed. Opt. 6, 129 (2013).

Köster, R. W.

D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, and V. Ntziachristos, Nat. Photonics 3, 412 (2009).
[CrossRef]

Langer, G.

Liu, T.

Loza-Alvarez, P.

S. Psilodimitrakopoulos, V. Petegnief, N. De Vera, O. Hernandez, D. Artigas, A. M. Planas, and P. Loza-Alvarez, Biophys. J. 104, 968 (2013).
[CrossRef]

S. Psilodimitrakopoulos, V. Petegnief, G. Soria, I. Amat-Roldan, D. Artigas, A. Planas, and P. Loza-Alvarez, Opt. Express 17, 14418 (2009).
[CrossRef]

Luo, W.

C. Vinegoni, T. Ralston, W. Tan, W. Luo, D. L. Marks, and S. A. Boppart, Appl. Phys. Lett. 88, 053901 (2006).
[CrossRef]

Ma, R.

R. Ma, S. Söntges, S. Shoham, V. Ntziachristos, and D. Razansky, Biomed. Opt. Express 3, 1724 (2012).
[CrossRef]

D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, and V. Ntziachristos, Nat. Photonics 3, 412 (2009).
[CrossRef]

Malone, C. J.

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, Biophys. J. 82, 493 (2002).
[CrossRef]

Marks, D. L.

C. Vinegoni, T. Ralston, W. Tan, W. Luo, D. L. Marks, and S. A. Boppart, Appl. Phys. Lett. 88, 053901 (2006).
[CrossRef]

Maslov, K.

Mazumder, N.

Megalou, E. V.

G. J. Tserevelakis, E. V. Megalou, G. Filippidis, B. Petanidou, C. Fotakis, and N. Tavernarakis, PLoS ONE 9, e84431 (2014).
[CrossRef]

Millard, A. C.

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, Biophys. J. 82, 493 (2002).
[CrossRef]

Mohler, W. A.

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, Biophys. J. 82, 493 (2002).
[CrossRef]

Ntziachristos, V.

M. Omar, J. Gateau, and V. Ntziachristos, Opt. Lett. 38, 2472 (2013).
[CrossRef]

R. Ma, S. Söntges, S. Shoham, V. Ntziachristos, and D. Razansky, Biomed. Opt. Express 3, 1724 (2012).
[CrossRef]

V. Ntziachristos, Nat. Methods 7, 603 (2010).
[CrossRef]

D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, and V. Ntziachristos, Nat. Photonics 3, 412 (2009).
[CrossRef]

Omar, M.

Pavone, F. S.

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, J. Biomed. Opt. 6, 129 (2013).

Perrimon, N.

D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, and V. Ntziachristos, Nat. Photonics 3, 412 (2009).
[CrossRef]

Petanidou, B.

G. J. Tserevelakis, E. V. Megalou, G. Filippidis, B. Petanidou, C. Fotakis, and N. Tavernarakis, PLoS ONE 9, e84431 (2014).
[CrossRef]

Petegnief, V.

S. Psilodimitrakopoulos, V. Petegnief, N. De Vera, O. Hernandez, D. Artigas, A. M. Planas, and P. Loza-Alvarez, Biophys. J. 104, 968 (2013).
[CrossRef]

S. Psilodimitrakopoulos, V. Petegnief, G. Soria, I. Amat-Roldan, D. Artigas, A. Planas, and P. Loza-Alvarez, Opt. Express 17, 14418 (2009).
[CrossRef]

Planas, A.

Planas, A. M.

S. Psilodimitrakopoulos, V. Petegnief, N. De Vera, O. Hernandez, D. Artigas, A. M. Planas, and P. Loza-Alvarez, Biophys. J. 104, 968 (2013).
[CrossRef]

Popp, J.

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, J. Biomed. Opt. 6, 129 (2013).

Psilodimitrakopoulos, S.

S. Psilodimitrakopoulos, V. Petegnief, N. De Vera, O. Hernandez, D. Artigas, A. M. Planas, and P. Loza-Alvarez, Biophys. J. 104, 968 (2013).
[CrossRef]

S. Psilodimitrakopoulos, V. Petegnief, G. Soria, I. Amat-Roldan, D. Artigas, A. Planas, and P. Loza-Alvarez, Opt. Express 17, 14418 (2009).
[CrossRef]

Puliafito, C. A.

Qiu, J.

Ralston, T.

C. Vinegoni, T. Ralston, W. Tan, W. Luo, D. L. Marks, and S. A. Boppart, Appl. Phys. Lett. 88, 053901 (2006).
[CrossRef]

Razansky, D.

R. Ma, S. Söntges, S. Shoham, V. Ntziachristos, and D. Razansky, Biomed. Opt. Express 3, 1724 (2012).
[CrossRef]

D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, and V. Ntziachristos, Nat. Photonics 3, 412 (2009).
[CrossRef]

Romero, C.

Shoham, S.

Söntges, S.

Soria, G.

Tan, W.

C. Vinegoni, T. Ralston, W. Tan, W. Luo, D. L. Marks, and S. A. Boppart, Appl. Phys. Lett. 88, 053901 (2006).
[CrossRef]

Tavernarakis, N.

G. J. Tserevelakis, E. V. Megalou, G. Filippidis, B. Petanidou, C. Fotakis, and N. Tavernarakis, PLoS ONE 9, e84431 (2014).
[CrossRef]

Terasaki, M.

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, Biophys. J. 82, 493 (2002).
[CrossRef]

Török, P.

Tserevelakis, G. J.

G. J. Tserevelakis, E. V. Megalou, G. Filippidis, B. Petanidou, C. Fotakis, and N. Tavernarakis, PLoS ONE 9, e84431 (2014).
[CrossRef]

Vinegoni, C.

D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, and V. Ntziachristos, Nat. Photonics 3, 412 (2009).
[CrossRef]

C. Vinegoni, T. Ralston, W. Tan, W. Luo, D. L. Marks, and S. A. Boppart, Appl. Phys. Lett. 88, 053901 (2006).
[CrossRef]

Vogler, N.

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, J. Biomed. Opt. 6, 129 (2013).

Wang, J.

Wang, L. V.

Wang, Y.

Wei, Q.

Xia, Y.

Xie, Z.

Zhang, H. F.

Zhang, X.

X. Zhang, H. F. Zhang, C. A. Puliafito, and S. Jiao, J. Biomed. Opt. 16, 080504 (2011).
[CrossRef]

Zhang, Y.

Appl. Phys. Lett. (1)

C. Vinegoni, T. Ralston, W. Tan, W. Luo, D. L. Marks, and S. A. Boppart, Appl. Phys. Lett. 88, 053901 (2006).
[CrossRef]

Biomed. Opt. Express (2)

Biophys. J. (2)

S. Psilodimitrakopoulos, V. Petegnief, N. De Vera, O. Hernandez, D. Artigas, A. M. Planas, and P. Loza-Alvarez, Biophys. J. 104, 968 (2013).
[CrossRef]

P. J. Campagnola, A. C. Millard, M. Terasaki, P. E. Hoppe, C. J. Malone, and W. A. Mohler, Biophys. J. 82, 493 (2002).
[CrossRef]

J. Biomed. Opt. (2)

R. Cicchi, N. Vogler, D. Kapsokalyvas, B. Dietzek, J. Popp, and F. S. Pavone, J. Biomed. Opt. 6, 129 (2013).

X. Zhang, H. F. Zhang, C. A. Puliafito, and S. Jiao, J. Biomed. Opt. 16, 080504 (2011).
[CrossRef]

Nat. Methods (1)

V. Ntziachristos, Nat. Methods 7, 603 (2010).
[CrossRef]

Nat. Photonics (1)

D. Razansky, M. Distel, C. Vinegoni, R. Ma, N. Perrimon, R. W. Köster, and V. Ntziachristos, Nat. Photonics 3, 412 (2009).
[CrossRef]

Opt. Express (3)

Opt. Lett. (3)

PLoS ONE (1)

G. J. Tserevelakis, E. V. Megalou, G. Filippidis, B. Petanidou, C. Fotakis, and N. Tavernarakis, PLoS ONE 9, e84431 (2014).
[CrossRef]

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Figures (4)

Fig. 1.
Fig. 1.

Schematic of the integrated MPOM. ND, neutral density filter; L, lens; M, mirror; P, pinhole; FMM, flip-mount mirror; PD, photodiode; GM, galvanometric mirror set; DM, dichroic mirror; SH, sample holder; BS, beam splitter; F, optical bandpass filter; PMT, photomultiplier tube; OL, objective lens; UTD, ultrasound transducer; A, amplifier; DAQ, data acquisition system.

Fig. 2.
Fig. 2.

Spatial resolution characterization of the multiphoton system. (a) Lateral profile of a 100 nm fluorescent nanobead with fitted Gaussian curve. (b) Axial profile of the nanobead. The insets show 2D images of the nanobead in the lateral and axial view.

Fig. 3.
Fig. 3.

Lateral resolution estimation of the OM. The graph shows the Gaussian fitted profile of a 2.8 μm microsphere. The inset illustrates the corresponding MAP of the sphere along the z axis.

Fig. 4.
Fig. 4.

Combined SHG and optoacoustic image of a zebrafish larva tail. (a) Hybrid image showing melanocytes (red) measured by the optoacoustic modality and muscle fibrils (green) recorded by the multiphoton system. (b) Brightfield image of the same tail region.

Equations (2)

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Rlateral=0.51λNA,
Rlateral,OM=dexp2dsph2,

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