Abstract

We developed handheld photoacoustic microscopy (PAM) to detect melanoma and determine tumor depth in nude mice in vivo. Compared to our previous PAM system for melanoma imaging, a new light delivery mechanism is introduced to improve light penetration. We show that melanomas with 4.1 and 3.7 mm thicknesses can be successfully detected in phantom and in in vivo experiments, respectively. With its deep melanoma imaging ability and handheld design, this system can be tested for clinical melanoma diagnosis, prognosis, and surgical planning for patients at the bedside.

© 2014 Optical Society of America

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2014 (1)

Y. Zhou, J. Yao, K. I. Maslov, and L. V. Wang, J. Biomed. Opt. 19, 37001 (2014).
[CrossRef]

2013 (4)

Y. Zhou, J. J. Yao, and L. H. V. Wang, Opt. Lett. 38, 2592 (2013).
[CrossRef]

E. M. Dunki-Jacobs, G. G. Callendar, and K. M. McMasters, Curr. Probl. Surg. 50, 351 (2013).
[CrossRef]

M. A. Calin, S. V. Parasca, R. Savastru, M. R. Calin, and S. Dontu, J. Cancer Res. Clin. Oncol. 139, 1083 (2013).
[CrossRef]

C. Zhang, Y. Zhou, C. Y. Li, and L. H. V. Wang, Appl. Phys. Lett. 102, 163702 (2013).
[CrossRef]

2012 (1)

L. H. V. Wang and S. Hu, Science 335, 1458 (2012).
[CrossRef]

2011 (2)

L. Smith and S. MacNeil, Skin Res. Technol. 17, 257 (2011).
[CrossRef]

P. Guitera and S. W. Menzies, Expert Rev. Anticancer Ther. 11, 715 (2011).
[CrossRef]

2010 (3)

K. M. Rubin, J. Dermatol. Nurses Assoc. 2, 6 (2010).
[CrossRef]

C. Kim, E. C. Cho, J. Chen, K. H. Song, L. Au, C. Favazza, Q. Zhang, C. M. Cobley, F. Gao, Y. Xia, and L. V. Wang, ACS Nano 4, 4559 (2010).
[CrossRef]

J. Staley, P. Grogan, A. K. Samadi, H. Cui, M. S. Cohen, and X. Yang, J. Biomed. Opt. 15, 040510 (2010).
[CrossRef]

2009 (4)

E. W. Stein, K. Maslov, and L. H. V. Wang, J. Appl. Phys. 105, 102027 (2009).
[CrossRef]

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

S. Segura, S. Puig, C. Carrera, J. Palou, and J. Malvehy, J. Am. Acad. Dermatol. 61, 216 (2009).
[CrossRef]

E. Dimitrow, M. Ziemer, M. J. Koehler, J. Norgauer, K. Konig, P. Elsner, and M. Kaatz, J. Invest. Dermatol. 129, 1752 (2009).
[CrossRef]

2007 (2)

C. Benvenuto-Andrade, S. W. Dusza, A. L. C. Agero, A. Scope, M. Rajadhyaksha, A. C. Halpern, and A. A. Marghoob, Arch. Dermatol. 143, 329 (2007).
[CrossRef]

T. Gambichler, P. Regeniter, F. G. Bechara, A. Orlikov, R. Vasa, G. Moussa, M. Stucker, P. Altmeyer, and K. Hoffmann, J. Am. Acad. Dermatol. 57, 629 (2007).
[CrossRef]

2006 (4)

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, Nat. Biotechnol. 24, 848 (2006).
[CrossRef]

J. Bittoun, B. Querleux, and L. Darrasse, NMR Biomed. 19, 723 (2006).

T. Z. Belhocine, A. M. Scott, E. Even-Sapir, J. L. Urbain, and R. Essner, J. Nucl. Med. 47, 957 (2006).

J. T. Oh, M. L. Li, H. F. Zhang, K. Maslov, G. Stoica, and L. H. V. Wang, J. Biomed. Opt. 11, 034032 (2006).
[CrossRef]

2003 (1)

A. C. Halpern, Semin. Cutan. Med. Surg. 22, 2 (2003).
[CrossRef]

2000 (1)

A. F. Jerant, J. T. Johnson, C. D. Sheridan, and T. J. Caffrey, Am. Fam. Physician 62, 357 (2000).

1998 (1)

I. H. Wolf, J. Smolle, H. P. Soyer, and H. Kerl, Melanoma Res. 8, 425 (1998).
[CrossRef]

1997 (1)

L. H. Wang, S. L. Jacques, and L. Q. Zheng, Comput. Methods Programs Biomed. 54, 141 (1997).
[CrossRef]

1995 (1)

W. Dummer, H. J. Blaheta, B. C. Bastian, T. Schenk, E. B. Brocher, and W. Remy, Arch. Dermatol. 131, 279 (1995).
[CrossRef]

1991 (1)

S. L. Jacques and D. J. Mcauliffe, Photochem. Photobiol. 53, 769 (1991).
[CrossRef]

Agero, A. L. C.

C. Benvenuto-Andrade, S. W. Dusza, A. L. C. Agero, A. Scope, M. Rajadhyaksha, A. C. Halpern, and A. A. Marghoob, Arch. Dermatol. 143, 329 (2007).
[CrossRef]

Altmeyer, P.

T. Gambichler, P. Regeniter, F. G. Bechara, A. Orlikov, R. Vasa, G. Moussa, M. Stucker, P. Altmeyer, and K. Hoffmann, J. Am. Acad. Dermatol. 57, 629 (2007).
[CrossRef]

Au, L.

C. Kim, E. C. Cho, J. Chen, K. H. Song, L. Au, C. Favazza, Q. Zhang, C. M. Cobley, F. Gao, Y. Xia, and L. V. Wang, ACS Nano 4, 4559 (2010).
[CrossRef]

Bastian, B. C.

W. Dummer, H. J. Blaheta, B. C. Bastian, T. Schenk, E. B. Brocher, and W. Remy, Arch. Dermatol. 131, 279 (1995).
[CrossRef]

Bechara, F. G.

T. Gambichler, P. Regeniter, F. G. Bechara, A. Orlikov, R. Vasa, G. Moussa, M. Stucker, P. Altmeyer, and K. Hoffmann, J. Am. Acad. Dermatol. 57, 629 (2007).
[CrossRef]

Belhocine, T. Z.

T. Z. Belhocine, A. M. Scott, E. Even-Sapir, J. L. Urbain, and R. Essner, J. Nucl. Med. 47, 957 (2006).

Benvenuto-Andrade, C.

C. Benvenuto-Andrade, S. W. Dusza, A. L. C. Agero, A. Scope, M. Rajadhyaksha, A. C. Halpern, and A. A. Marghoob, Arch. Dermatol. 143, 329 (2007).
[CrossRef]

Bittoun, J.

J. Bittoun, B. Querleux, and L. Darrasse, NMR Biomed. 19, 723 (2006).

Blaheta, H. J.

W. Dummer, H. J. Blaheta, B. C. Bastian, T. Schenk, E. B. Brocher, and W. Remy, Arch. Dermatol. 131, 279 (1995).
[CrossRef]

Brocher, E. B.

W. Dummer, H. J. Blaheta, B. C. Bastian, T. Schenk, E. B. Brocher, and W. Remy, Arch. Dermatol. 131, 279 (1995).
[CrossRef]

Caffrey, T. J.

A. F. Jerant, J. T. Johnson, C. D. Sheridan, and T. J. Caffrey, Am. Fam. Physician 62, 357 (2000).

Calin, M. A.

M. A. Calin, S. V. Parasca, R. Savastru, M. R. Calin, and S. Dontu, J. Cancer Res. Clin. Oncol. 139, 1083 (2013).
[CrossRef]

Calin, M. R.

M. A. Calin, S. V. Parasca, R. Savastru, M. R. Calin, and S. Dontu, J. Cancer Res. Clin. Oncol. 139, 1083 (2013).
[CrossRef]

Callendar, G. G.

E. M. Dunki-Jacobs, G. G. Callendar, and K. M. McMasters, Curr. Probl. Surg. 50, 351 (2013).
[CrossRef]

Carrera, C.

S. Segura, S. Puig, C. Carrera, J. Palou, and J. Malvehy, J. Am. Acad. Dermatol. 61, 216 (2009).
[CrossRef]

Chen, J.

C. Kim, E. C. Cho, J. Chen, K. H. Song, L. Au, C. Favazza, Q. Zhang, C. M. Cobley, F. Gao, Y. Xia, and L. V. Wang, ACS Nano 4, 4559 (2010).
[CrossRef]

Cho, E. C.

C. Kim, E. C. Cho, J. Chen, K. H. Song, L. Au, C. Favazza, Q. Zhang, C. M. Cobley, F. Gao, Y. Xia, and L. V. Wang, ACS Nano 4, 4559 (2010).
[CrossRef]

Cobley, C. M.

C. Kim, E. C. Cho, J. Chen, K. H. Song, L. Au, C. Favazza, Q. Zhang, C. M. Cobley, F. Gao, Y. Xia, and L. V. Wang, ACS Nano 4, 4559 (2010).
[CrossRef]

Cohen, M. S.

J. Staley, P. Grogan, A. K. Samadi, H. Cui, M. S. Cohen, and X. Yang, J. Biomed. Opt. 15, 040510 (2010).
[CrossRef]

Cui, H.

J. Staley, P. Grogan, A. K. Samadi, H. Cui, M. S. Cohen, and X. Yang, J. Biomed. Opt. 15, 040510 (2010).
[CrossRef]

Darrasse, L.

J. Bittoun, B. Querleux, and L. Darrasse, NMR Biomed. 19, 723 (2006).

Dimitrow, E.

E. Dimitrow, M. Ziemer, M. J. Koehler, J. Norgauer, K. Konig, P. Elsner, and M. Kaatz, J. Invest. Dermatol. 129, 1752 (2009).
[CrossRef]

Distel, M.

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

Dontu, S.

M. A. Calin, S. V. Parasca, R. Savastru, M. R. Calin, and S. Dontu, J. Cancer Res. Clin. Oncol. 139, 1083 (2013).
[CrossRef]

Dummer, W.

W. Dummer, H. J. Blaheta, B. C. Bastian, T. Schenk, E. B. Brocher, and W. Remy, Arch. Dermatol. 131, 279 (1995).
[CrossRef]

Dunki-Jacobs, E. M.

E. M. Dunki-Jacobs, G. G. Callendar, and K. M. McMasters, Curr. Probl. Surg. 50, 351 (2013).
[CrossRef]

Dusza, S. W.

C. Benvenuto-Andrade, S. W. Dusza, A. L. C. Agero, A. Scope, M. Rajadhyaksha, A. C. Halpern, and A. A. Marghoob, Arch. Dermatol. 143, 329 (2007).
[CrossRef]

Elsner, P.

E. Dimitrow, M. Ziemer, M. J. Koehler, J. Norgauer, K. Konig, P. Elsner, and M. Kaatz, J. Invest. Dermatol. 129, 1752 (2009).
[CrossRef]

Essner, R.

T. Z. Belhocine, A. M. Scott, E. Even-Sapir, J. L. Urbain, and R. Essner, J. Nucl. Med. 47, 957 (2006).

Even-Sapir, E.

T. Z. Belhocine, A. M. Scott, E. Even-Sapir, J. L. Urbain, and R. Essner, J. Nucl. Med. 47, 957 (2006).

Favazza, C.

C. Kim, E. C. Cho, J. Chen, K. H. Song, L. Au, C. Favazza, Q. Zhang, C. M. Cobley, F. Gao, Y. Xia, and L. V. Wang, ACS Nano 4, 4559 (2010).
[CrossRef]

Gambichler, T.

T. Gambichler, P. Regeniter, F. G. Bechara, A. Orlikov, R. Vasa, G. Moussa, M. Stucker, P. Altmeyer, and K. Hoffmann, J. Am. Acad. Dermatol. 57, 629 (2007).
[CrossRef]

Gao, F.

C. Kim, E. C. Cho, J. Chen, K. H. Song, L. Au, C. Favazza, Q. Zhang, C. M. Cobley, F. Gao, Y. Xia, and L. V. Wang, ACS Nano 4, 4559 (2010).
[CrossRef]

Grogan, P.

J. Staley, P. Grogan, A. K. Samadi, H. Cui, M. S. Cohen, and X. Yang, J. Biomed. Opt. 15, 040510 (2010).
[CrossRef]

Guitera, P.

P. Guitera and S. W. Menzies, Expert Rev. Anticancer Ther. 11, 715 (2011).
[CrossRef]

Halpern, A. C.

C. Benvenuto-Andrade, S. W. Dusza, A. L. C. Agero, A. Scope, M. Rajadhyaksha, A. C. Halpern, and A. A. Marghoob, Arch. Dermatol. 143, 329 (2007).
[CrossRef]

A. C. Halpern, Semin. Cutan. Med. Surg. 22, 2 (2003).
[CrossRef]

Hoffmann, K.

T. Gambichler, P. Regeniter, F. G. Bechara, A. Orlikov, R. Vasa, G. Moussa, M. Stucker, P. Altmeyer, and K. Hoffmann, J. Am. Acad. Dermatol. 57, 629 (2007).
[CrossRef]

Hu, S.

L. H. V. Wang and S. Hu, Science 335, 1458 (2012).
[CrossRef]

Jacques, S. L.

L. H. Wang, S. L. Jacques, and L. Q. Zheng, Comput. Methods Programs Biomed. 54, 141 (1997).
[CrossRef]

S. L. Jacques and D. J. Mcauliffe, Photochem. Photobiol. 53, 769 (1991).
[CrossRef]

Jerant, A. F.

A. F. Jerant, J. T. Johnson, C. D. Sheridan, and T. J. Caffrey, Am. Fam. Physician 62, 357 (2000).

Johnson, J. T.

A. F. Jerant, J. T. Johnson, C. D. Sheridan, and T. J. Caffrey, Am. Fam. Physician 62, 357 (2000).

Kaatz, M.

E. Dimitrow, M. Ziemer, M. J. Koehler, J. Norgauer, K. Konig, P. Elsner, and M. Kaatz, J. Invest. Dermatol. 129, 1752 (2009).
[CrossRef]

Kerl, H.

I. H. Wolf, J. Smolle, H. P. Soyer, and H. Kerl, Melanoma Res. 8, 425 (1998).
[CrossRef]

Kim, C.

C. Kim, E. C. Cho, J. Chen, K. H. Song, L. Au, C. Favazza, Q. Zhang, C. M. Cobley, F. Gao, Y. Xia, and L. V. Wang, ACS Nano 4, 4559 (2010).
[CrossRef]

Koehler, M. J.

E. Dimitrow, M. Ziemer, M. J. Koehler, J. Norgauer, K. Konig, P. Elsner, and M. Kaatz, J. Invest. Dermatol. 129, 1752 (2009).
[CrossRef]

Konig, K.

E. Dimitrow, M. Ziemer, M. J. Koehler, J. Norgauer, K. Konig, P. Elsner, and M. Kaatz, J. Invest. Dermatol. 129, 1752 (2009).
[CrossRef]

Koster, R. W.

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

Li, C. Y.

C. Zhang, Y. Zhou, C. Y. Li, and L. H. V. Wang, Appl. Phys. Lett. 102, 163702 (2013).
[CrossRef]

Li, M. L.

J. T. Oh, M. L. Li, H. F. Zhang, K. Maslov, G. Stoica, and L. H. V. Wang, J. Biomed. Opt. 11, 034032 (2006).
[CrossRef]

Ma, R.

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

MacNeil, S.

L. Smith and S. MacNeil, Skin Res. Technol. 17, 257 (2011).
[CrossRef]

Malvehy, J.

S. Segura, S. Puig, C. Carrera, J. Palou, and J. Malvehy, J. Am. Acad. Dermatol. 61, 216 (2009).
[CrossRef]

Marghoob, A. A.

C. Benvenuto-Andrade, S. W. Dusza, A. L. C. Agero, A. Scope, M. Rajadhyaksha, A. C. Halpern, and A. A. Marghoob, Arch. Dermatol. 143, 329 (2007).
[CrossRef]

Maslov, K.

E. W. Stein, K. Maslov, and L. H. V. Wang, J. Appl. Phys. 105, 102027 (2009).
[CrossRef]

J. T. Oh, M. L. Li, H. F. Zhang, K. Maslov, G. Stoica, and L. H. V. Wang, J. Biomed. Opt. 11, 034032 (2006).
[CrossRef]

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, Nat. Biotechnol. 24, 848 (2006).
[CrossRef]

Maslov, K. I.

Y. Zhou, J. Yao, K. I. Maslov, and L. V. Wang, J. Biomed. Opt. 19, 37001 (2014).
[CrossRef]

Mcauliffe, D. J.

S. L. Jacques and D. J. Mcauliffe, Photochem. Photobiol. 53, 769 (1991).
[CrossRef]

McMasters, K. M.

E. M. Dunki-Jacobs, G. G. Callendar, and K. M. McMasters, Curr. Probl. Surg. 50, 351 (2013).
[CrossRef]

Menzies, S. W.

P. Guitera and S. W. Menzies, Expert Rev. Anticancer Ther. 11, 715 (2011).
[CrossRef]

Moussa, G.

T. Gambichler, P. Regeniter, F. G. Bechara, A. Orlikov, R. Vasa, G. Moussa, M. Stucker, P. Altmeyer, and K. Hoffmann, J. Am. Acad. Dermatol. 57, 629 (2007).
[CrossRef]

Norgauer, J.

E. Dimitrow, M. Ziemer, M. J. Koehler, J. Norgauer, K. Konig, P. Elsner, and M. Kaatz, J. Invest. Dermatol. 129, 1752 (2009).
[CrossRef]

Ntziachristos, V.

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

Oh, J. T.

J. T. Oh, M. L. Li, H. F. Zhang, K. Maslov, G. Stoica, and L. H. V. Wang, J. Biomed. Opt. 11, 034032 (2006).
[CrossRef]

Orlikov, A.

T. Gambichler, P. Regeniter, F. G. Bechara, A. Orlikov, R. Vasa, G. Moussa, M. Stucker, P. Altmeyer, and K. Hoffmann, J. Am. Acad. Dermatol. 57, 629 (2007).
[CrossRef]

Palou, J.

S. Segura, S. Puig, C. Carrera, J. Palou, and J. Malvehy, J. Am. Acad. Dermatol. 61, 216 (2009).
[CrossRef]

Parasca, S. V.

M. A. Calin, S. V. Parasca, R. Savastru, M. R. Calin, and S. Dontu, J. Cancer Res. Clin. Oncol. 139, 1083 (2013).
[CrossRef]

Perrimon, N.

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

Puig, S.

S. Segura, S. Puig, C. Carrera, J. Palou, and J. Malvehy, J. Am. Acad. Dermatol. 61, 216 (2009).
[CrossRef]

Querleux, B.

J. Bittoun, B. Querleux, and L. Darrasse, NMR Biomed. 19, 723 (2006).

Rajadhyaksha, M.

C. Benvenuto-Andrade, S. W. Dusza, A. L. C. Agero, A. Scope, M. Rajadhyaksha, A. C. Halpern, and A. A. Marghoob, Arch. Dermatol. 143, 329 (2007).
[CrossRef]

Razansky, D.

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

Regeniter, P.

T. Gambichler, P. Regeniter, F. G. Bechara, A. Orlikov, R. Vasa, G. Moussa, M. Stucker, P. Altmeyer, and K. Hoffmann, J. Am. Acad. Dermatol. 57, 629 (2007).
[CrossRef]

Remy, W.

W. Dummer, H. J. Blaheta, B. C. Bastian, T. Schenk, E. B. Brocher, and W. Remy, Arch. Dermatol. 131, 279 (1995).
[CrossRef]

Rubin, K. M.

K. M. Rubin, J. Dermatol. Nurses Assoc. 2, 6 (2010).
[CrossRef]

Samadi, A. K.

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T. Z. Belhocine, A. M. Scott, E. Even-Sapir, J. L. Urbain, and R. Essner, J. Nucl. Med. 47, 957 (2006).

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Figures (5)

Fig. 1.
Fig. 1.

Experimental handheld photoacoustic microscopy (PAM) system. (a) Schematic of the handheld PAM system. (b) Components held by the translation stage in the handheld probe. (c) Photograph of the handheld probe.

Fig. 2.
Fig. 2.

Monte Carlo simulations of the old and new PAM systems for melanoma imaging. Melanoma phantom and light illumination methods used in the simulations of (a) the old and (b) the new systems. The red arrows show the incident angles and areas of the light used in the Monte Carlo simulations. Specific heat absorption (Ae) distributions in (c) the old and (d) the new PAM systems with the same incident energy. (e) Averaged Ae in the black-dashed-square areas [shown in (a)–(d)] at the bottom boundary of the melanoma phantoms in (c) blue line and (d) red dotted line, showing that the melanoma is much more strongly illuminated at the bottom boundary using the new PAM system.

Fig. 3.
Fig. 3.

Spatial resolutions of the current PAM system. PA amplitudes in (a) the lateral x and (b) the axial z directions. The full widths at half-maximum are 230 μm in (a) and 59 μm in (b).

Fig. 4.
Fig. 4.

Handheld PAM of melanoma phantoms. Photos of melanoma phantoms with different diameters [(a) 7 mm, (b) 9.5 mm, and (c) 14 mm]. (a1)–(a4), (b1)–(b4), and (c1)–(c4): PAM images of different thicknesses of melanoma phantoms with the same diameter as in (a), (b), and (c), respectively. (d) Measured thicknesses of melanoma phantoms versus preset thicknesses.

Fig. 5.
Fig. 5.

Handheld PAM of melanoma in a nude mouse in vivo. (a) PAM image of the melanoma clearly showing both the top and bottom boundaries. (b) The same PAM image as (a). The red dots outline the melanoma according to the shape of the excised melanoma (red dots) in its photograph (c). Photograph of the melanoma taken in vivo (d).

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