Abstract

Photoacoustic microscopy is predominantly sensitive to optical absorption, while optical coherence tomography relies on optical backscattering. Integrating their complementary contrasts can provide comprehensive information about biological tissue. We have developed a dual-modality microscope that combines the two for studying microcirculation. Three-dimensional imaging of microvasculature and its local environment has been demonstrated at micrometer-order resolution using endogenous contrast in vivo.

© 2009 OSA

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2009

2008

K. Maslov, H. F. Zhang, S. Hu, and L. V. Wang, “Optical-resolution photoacoustic microscopy for in vivo imaging of single capillaries,” Opt. Lett. 33(9), 929–931 (2008).
[CrossRef] [PubMed]

L. V. Wang, “Prospects of photoacoustic tomography,” Med. Phys. 35(12), 5758–5767 (2008).
[CrossRef]

L. V. Wang, “Tutorial on photoacoustic microscopy and computed tomography,” IEEE J. Sel. Top. Quantum Electron. 14(1), 171–179 (2008).
[CrossRef]

2007

H. F. Zhang, K. Maslov, and L. V. Wang, “In vivo imaging of subcutaneous structures using functional photoacoustic microscopy,” Nat. Protocols 2(4), 797–804 (2007).
[CrossRef]

H. F. Zhang, K. Maslov, M. Sivaramakrishnan, G. Stoica, and L. V. Wang, “Imaging of hemoglobin oxygen saturation variations in single vessels in vivo using photoacoustic microscopy,” Appl. Phys. Lett. 90(5), 053901 (2007).
[CrossRef]

2006

J. Oh, M. Li, H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Three-dimensional imaging of skin melanoma in vivo by dual-wavelength photoacoustic microscopy,” J. Biomed. Opt. 11(3), 034032 (2006).
[CrossRef]

C. Vinegoni, T. Ralston, W. Tan, W. Luo, D. L. Marks, and S. A. Boppart, “Integrated structural and functional optical imaging combining spectral-domain optical coherence and multiphoton microscopy,” Appl. Phys. Lett. 88(5), 053901 (2006).
[CrossRef]

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[CrossRef] [PubMed]

2005

J. J. Niederhauser, M. Jaeger, R. Lemor, P. Weber, and M. Frenz, “Combined ultrasound and optoacoustic system for real-time high-contrast vascular imaging in vivo,” IEEE Trans. Med. Imaging 24(4), 436–440 (2005).
[CrossRef] [PubMed]

J. Ai and L. V. Wang, “Synchronous self-elimination of autocorrelation interference in Fourier-domain optical coherence tomography,” Opt. Lett. 30(21), 2939–2941 (2005).
[CrossRef] [PubMed]

2004

2002

R. K. Jain, L. L. Munn, and D. Fukumura, “Dissecting tumour pathophysiology using intravital microscopy,” Nat. Rev. Cancer 2(4), 266–276 (2002).
[CrossRef] [PubMed]

2001

E. B. Brown, R. B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, and R. K. Jain, “In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy,” Nat. Med. 7(7), 864–868 (2001).
[CrossRef] [PubMed]

2000

1999

R. G. Nadeau, W. Groner, J. W. Winkelman, A. G. Harris, C. Ince, G. J. Bouma, and K. Messmer, “Orthogonal polarization spectral imaging: a new method for study of the microcirculation,” Nat. Med. 5(10), 1209–1212 (1999).
[CrossRef] [PubMed]

J. Seylaz, R. Charbonné, K. Nanri, D. Von Euw, J. Borredon, K. Kacem, P. Méric, and E. Pinard, “Dynamic in vivo measurement of erythrocyte velocity and flow in capillaries and of microvessel diameter in the rat brain by confocal laser microscopy,” J. Cereb. Blood Flow Metab. 19(8), 863–870 (1999).
[CrossRef] [PubMed]

1997

B. Fagrell and M. Intaglietta, “Microcirculation: its significance in clinical and molecular medicine,” J. Intern. Med. 241(5), 349–362 (1997).
[CrossRef] [PubMed]

1980

E. Eriksson, J. V. Boykin, and R. N. Pittman, “Method for in vivo microscopy of the cutaneous microcirculation of the hairless mouse ear,” Microvasc. Res. 19(3), 374–379 (1980).
[CrossRef] [PubMed]

Ai, J.

Boppart, S. A.

C. Vinegoni, T. Ralston, W. Tan, W. Luo, D. L. Marks, and S. A. Boppart, “Integrated structural and functional optical imaging combining spectral-domain optical coherence and multiphoton microscopy,” Appl. Phys. Lett. 88(5), 053901 (2006).
[CrossRef]

Borredon, J.

J. Seylaz, R. Charbonné, K. Nanri, D. Von Euw, J. Borredon, K. Kacem, P. Méric, and E. Pinard, “Dynamic in vivo measurement of erythrocyte velocity and flow in capillaries and of microvessel diameter in the rat brain by confocal laser microscopy,” J. Cereb. Blood Flow Metab. 19(8), 863–870 (1999).
[CrossRef] [PubMed]

Bouma, B. E.

Bouma, G. J.

R. G. Nadeau, W. Groner, J. W. Winkelman, A. G. Harris, C. Ince, G. J. Bouma, and K. Messmer, “Orthogonal polarization spectral imaging: a new method for study of the microcirculation,” Nat. Med. 5(10), 1209–1212 (1999).
[CrossRef] [PubMed]

Boykin, J. V.

E. Eriksson, J. V. Boykin, and R. N. Pittman, “Method for in vivo microscopy of the cutaneous microcirculation of the hairless mouse ear,” Microvasc. Res. 19(3), 374–379 (1980).
[CrossRef] [PubMed]

Brown, E. B.

E. B. Brown, R. B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, and R. K. Jain, “In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy,” Nat. Med. 7(7), 864–868 (2001).
[CrossRef] [PubMed]

Buhman, K. K.

Campbell, R. B.

E. B. Brown, R. B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, and R. K. Jain, “In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy,” Nat. Med. 7(7), 864–868 (2001).
[CrossRef] [PubMed]

Carmeliet, P.

E. B. Brown, R. B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, and R. K. Jain, “In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy,” Nat. Med. 7(7), 864–868 (2001).
[CrossRef] [PubMed]

Cense, B.

Charbonné, R.

J. Seylaz, R. Charbonné, K. Nanri, D. Von Euw, J. Borredon, K. Kacem, P. Méric, and E. Pinard, “Dynamic in vivo measurement of erythrocyte velocity and flow in capillaries and of microvessel diameter in the rat brain by confocal laser microscopy,” J. Cereb. Blood Flow Metab. 19(8), 863–870 (1999).
[CrossRef] [PubMed]

Chen, H. T.

Chen, T. C.

Chen, Z.

Cheng, J. X.

de Boer, J. F.

Eriksson, E.

E. Eriksson, J. V. Boykin, and R. N. Pittman, “Method for in vivo microscopy of the cutaneous microcirculation of the hairless mouse ear,” Microvasc. Res. 19(3), 374–379 (1980).
[CrossRef] [PubMed]

Fagrell, B.

B. Fagrell and M. Intaglietta, “Microcirculation: its significance in clinical and molecular medicine,” J. Intern. Med. 241(5), 349–362 (1997).
[CrossRef] [PubMed]

Frenz, M.

J. J. Niederhauser, M. Jaeger, R. Lemor, P. Weber, and M. Frenz, “Combined ultrasound and optoacoustic system for real-time high-contrast vascular imaging in vivo,” IEEE Trans. Med. Imaging 24(4), 436–440 (2005).
[CrossRef] [PubMed]

Fukumura, D.

R. K. Jain, L. L. Munn, and D. Fukumura, “Dissecting tumour pathophysiology using intravital microscopy,” Nat. Rev. Cancer 2(4), 266–276 (2002).
[CrossRef] [PubMed]

E. B. Brown, R. B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, and R. K. Jain, “In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy,” Nat. Med. 7(7), 864–868 (2001).
[CrossRef] [PubMed]

Groner, W.

R. G. Nadeau, W. Groner, J. W. Winkelman, A. G. Harris, C. Ince, G. J. Bouma, and K. Messmer, “Orthogonal polarization spectral imaging: a new method for study of the microcirculation,” Nat. Med. 5(10), 1209–1212 (1999).
[CrossRef] [PubMed]

Harris, A. G.

R. G. Nadeau, W. Groner, J. W. Winkelman, A. G. Harris, C. Ince, G. J. Bouma, and K. Messmer, “Orthogonal polarization spectral imaging: a new method for study of the microcirculation,” Nat. Med. 5(10), 1209–1212 (1999).
[CrossRef] [PubMed]

Hu, S.

Ince, C.

R. G. Nadeau, W. Groner, J. W. Winkelman, A. G. Harris, C. Ince, G. J. Bouma, and K. Messmer, “Orthogonal polarization spectral imaging: a new method for study of the microcirculation,” Nat. Med. 5(10), 1209–1212 (1999).
[CrossRef] [PubMed]

Intaglietta, M.

B. Fagrell and M. Intaglietta, “Microcirculation: its significance in clinical and molecular medicine,” J. Intern. Med. 241(5), 349–362 (1997).
[CrossRef] [PubMed]

Jaeger, M.

J. J. Niederhauser, M. Jaeger, R. Lemor, P. Weber, and M. Frenz, “Combined ultrasound and optoacoustic system for real-time high-contrast vascular imaging in vivo,” IEEE Trans. Med. Imaging 24(4), 436–440 (2005).
[CrossRef] [PubMed]

Jain, R. K.

R. K. Jain, L. L. Munn, and D. Fukumura, “Dissecting tumour pathophysiology using intravital microscopy,” Nat. Rev. Cancer 2(4), 266–276 (2002).
[CrossRef] [PubMed]

E. B. Brown, R. B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, and R. K. Jain, “In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy,” Nat. Med. 7(7), 864–868 (2001).
[CrossRef] [PubMed]

Jung, Y. K.

Kacem, K.

J. Seylaz, R. Charbonné, K. Nanri, D. Von Euw, J. Borredon, K. Kacem, P. Méric, and E. Pinard, “Dynamic in vivo measurement of erythrocyte velocity and flow in capillaries and of microvessel diameter in the rat brain by confocal laser microscopy,” J. Cereb. Blood Flow Metab. 19(8), 863–870 (1999).
[CrossRef] [PubMed]

Ku, G.

G. Ku, K. Maslov, L. Li, and L. V. Wang, “Photoacoustic microscopy with 2-µm transverse resolution,” J. Biomed. Opt. under review.
[PubMed]

Lemor, R.

J. J. Niederhauser, M. Jaeger, R. Lemor, P. Weber, and M. Frenz, “Combined ultrasound and optoacoustic system for real-time high-contrast vascular imaging in vivo,” IEEE Trans. Med. Imaging 24(4), 436–440 (2005).
[CrossRef] [PubMed]

Li, L.

G. Ku, K. Maslov, L. Li, and L. V. Wang, “Photoacoustic microscopy with 2-µm transverse resolution,” J. Biomed. Opt. under review.
[PubMed]

Li, M.

J. Oh, M. Li, H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Three-dimensional imaging of skin melanoma in vivo by dual-wavelength photoacoustic microscopy,” J. Biomed. Opt. 11(3), 034032 (2006).
[CrossRef]

Luo, W.

C. Vinegoni, T. Ralston, W. Tan, W. Luo, D. L. Marks, and S. A. Boppart, “Integrated structural and functional optical imaging combining spectral-domain optical coherence and multiphoton microscopy,” Appl. Phys. Lett. 88(5), 053901 (2006).
[CrossRef]

Marks, D. L.

C. Vinegoni, T. Ralston, W. Tan, W. Luo, D. L. Marks, and S. A. Boppart, “Integrated structural and functional optical imaging combining spectral-domain optical coherence and multiphoton microscopy,” Appl. Phys. Lett. 88(5), 053901 (2006).
[CrossRef]

Maslov, K.

K. Maslov, H. F. Zhang, S. Hu, and L. V. Wang, “Optical-resolution photoacoustic microscopy for in vivo imaging of single capillaries,” Opt. Lett. 33(9), 929–931 (2008).
[CrossRef] [PubMed]

H. F. Zhang, K. Maslov, and L. V. Wang, “In vivo imaging of subcutaneous structures using functional photoacoustic microscopy,” Nat. Protocols 2(4), 797–804 (2007).
[CrossRef]

H. F. Zhang, K. Maslov, M. Sivaramakrishnan, G. Stoica, and L. V. Wang, “Imaging of hemoglobin oxygen saturation variations in single vessels in vivo using photoacoustic microscopy,” Appl. Phys. Lett. 90(5), 053901 (2007).
[CrossRef]

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[CrossRef] [PubMed]

J. Oh, M. Li, H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Three-dimensional imaging of skin melanoma in vivo by dual-wavelength photoacoustic microscopy,” J. Biomed. Opt. 11(3), 034032 (2006).
[CrossRef]

G. Ku, K. Maslov, L. Li, and L. V. Wang, “Photoacoustic microscopy with 2-µm transverse resolution,” J. Biomed. Opt. under review.
[PubMed]

Méric, P.

J. Seylaz, R. Charbonné, K. Nanri, D. Von Euw, J. Borredon, K. Kacem, P. Méric, and E. Pinard, “Dynamic in vivo measurement of erythrocyte velocity and flow in capillaries and of microvessel diameter in the rat brain by confocal laser microscopy,” J. Cereb. Blood Flow Metab. 19(8), 863–870 (1999).
[CrossRef] [PubMed]

Messmer, K.

R. G. Nadeau, W. Groner, J. W. Winkelman, A. G. Harris, C. Ince, G. J. Bouma, and K. Messmer, “Orthogonal polarization spectral imaging: a new method for study of the microcirculation,” Nat. Med. 5(10), 1209–1212 (1999).
[CrossRef] [PubMed]

Munn, L. L.

R. K. Jain, L. L. Munn, and D. Fukumura, “Dissecting tumour pathophysiology using intravital microscopy,” Nat. Rev. Cancer 2(4), 266–276 (2002).
[CrossRef] [PubMed]

Nadeau, R. G.

R. G. Nadeau, W. Groner, J. W. Winkelman, A. G. Harris, C. Ince, G. J. Bouma, and K. Messmer, “Orthogonal polarization spectral imaging: a new method for study of the microcirculation,” Nat. Med. 5(10), 1209–1212 (1999).
[CrossRef] [PubMed]

Nanri, K.

J. Seylaz, R. Charbonné, K. Nanri, D. Von Euw, J. Borredon, K. Kacem, P. Méric, and E. Pinard, “Dynamic in vivo measurement of erythrocyte velocity and flow in capillaries and of microvessel diameter in the rat brain by confocal laser microscopy,” J. Cereb. Blood Flow Metab. 19(8), 863–870 (1999).
[CrossRef] [PubMed]

Nassif, N. A.

Nelson, J. S.

Niederhauser, J. J.

J. J. Niederhauser, M. Jaeger, R. Lemor, P. Weber, and M. Frenz, “Combined ultrasound and optoacoustic system for real-time high-contrast vascular imaging in vivo,” IEEE Trans. Med. Imaging 24(4), 436–440 (2005).
[CrossRef] [PubMed]

Oh, J.

J. Oh, M. Li, H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Three-dimensional imaging of skin melanoma in vivo by dual-wavelength photoacoustic microscopy,” J. Biomed. Opt. 11(3), 034032 (2006).
[CrossRef]

Park, B. H.

Pierce, M. C.

Pinard, E.

J. Seylaz, R. Charbonné, K. Nanri, D. Von Euw, J. Borredon, K. Kacem, P. Méric, and E. Pinard, “Dynamic in vivo measurement of erythrocyte velocity and flow in capillaries and of microvessel diameter in the rat brain by confocal laser microscopy,” J. Cereb. Blood Flow Metab. 19(8), 863–870 (1999).
[CrossRef] [PubMed]

Pittman, R. N.

E. Eriksson, J. V. Boykin, and R. N. Pittman, “Method for in vivo microscopy of the cutaneous microcirculation of the hairless mouse ear,” Microvasc. Res. 19(3), 374–379 (1980).
[CrossRef] [PubMed]

Ralston, T.

C. Vinegoni, T. Ralston, W. Tan, W. Luo, D. L. Marks, and S. A. Boppart, “Integrated structural and functional optical imaging combining spectral-domain optical coherence and multiphoton microscopy,” Appl. Phys. Lett. 88(5), 053901 (2006).
[CrossRef]

Saxer, C.

Seylaz, J.

J. Seylaz, R. Charbonné, K. Nanri, D. Von Euw, J. Borredon, K. Kacem, P. Méric, and E. Pinard, “Dynamic in vivo measurement of erythrocyte velocity and flow in capillaries and of microvessel diameter in the rat brain by confocal laser microscopy,” J. Cereb. Blood Flow Metab. 19(8), 863–870 (1999).
[CrossRef] [PubMed]

Shi, Y. Z.

Sivaramakrishnan, M.

H. F. Zhang, K. Maslov, M. Sivaramakrishnan, G. Stoica, and L. V. Wang, “Imaging of hemoglobin oxygen saturation variations in single vessels in vivo using photoacoustic microscopy,” Appl. Phys. Lett. 90(5), 053901 (2007).
[CrossRef]

Slipchenko, M. N.

Stoica, G.

H. F. Zhang, K. Maslov, M. Sivaramakrishnan, G. Stoica, and L. V. Wang, “Imaging of hemoglobin oxygen saturation variations in single vessels in vivo using photoacoustic microscopy,” Appl. Phys. Lett. 90(5), 053901 (2007).
[CrossRef]

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[CrossRef] [PubMed]

J. Oh, M. Li, H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Three-dimensional imaging of skin melanoma in vivo by dual-wavelength photoacoustic microscopy,” J. Biomed. Opt. 11(3), 034032 (2006).
[CrossRef]

Tan, W.

C. Vinegoni, T. Ralston, W. Tan, W. Luo, D. L. Marks, and S. A. Boppart, “Integrated structural and functional optical imaging combining spectral-domain optical coherence and multiphoton microscopy,” Appl. Phys. Lett. 88(5), 053901 (2006).
[CrossRef]

Tearney, G. J.

Tsuzuki, Y.

E. B. Brown, R. B. Campbell, Y. Tsuzuki, L. Xu, P. Carmeliet, D. Fukumura, and R. K. Jain, “In vivo measurement of gene expression, angiogenesis and physiological function in tumors using multiphoton laser scanning microscopy,” Nat. Med. 7(7), 864–868 (2001).
[CrossRef] [PubMed]

Vinegoni, C.

C. Vinegoni, T. Ralston, W. Tan, W. Luo, D. L. Marks, and S. A. Boppart, “Integrated structural and functional optical imaging combining spectral-domain optical coherence and multiphoton microscopy,” Appl. Phys. Lett. 88(5), 053901 (2006).
[CrossRef]

Von Euw, D.

J. Seylaz, R. Charbonné, K. Nanri, D. Von Euw, J. Borredon, K. Kacem, P. Méric, and E. Pinard, “Dynamic in vivo measurement of erythrocyte velocity and flow in capillaries and of microvessel diameter in the rat brain by confocal laser microscopy,” J. Cereb. Blood Flow Metab. 19(8), 863–870 (1999).
[CrossRef] [PubMed]

Wang, H. F.

Wang, L. V.

K. Maslov, H. F. Zhang, S. Hu, and L. V. Wang, “Optical-resolution photoacoustic microscopy for in vivo imaging of single capillaries,” Opt. Lett. 33(9), 929–931 (2008).
[CrossRef] [PubMed]

L. V. Wang, “Tutorial on photoacoustic microscopy and computed tomography,” IEEE J. Sel. Top. Quantum Electron. 14(1), 171–179 (2008).
[CrossRef]

L. V. Wang, “Prospects of photoacoustic tomography,” Med. Phys. 35(12), 5758–5767 (2008).
[CrossRef]

H. F. Zhang, K. Maslov, M. Sivaramakrishnan, G. Stoica, and L. V. Wang, “Imaging of hemoglobin oxygen saturation variations in single vessels in vivo using photoacoustic microscopy,” Appl. Phys. Lett. 90(5), 053901 (2007).
[CrossRef]

H. F. Zhang, K. Maslov, and L. V. Wang, “In vivo imaging of subcutaneous structures using functional photoacoustic microscopy,” Nat. Protocols 2(4), 797–804 (2007).
[CrossRef]

H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Functional photoacoustic microscopy for high-resolution and noninvasive in vivo imaging,” Nat. Biotechnol. 24(7), 848–851 (2006).
[CrossRef] [PubMed]

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Figures (4)

Fig. 1
Fig. 1

Schematic of the combined photoacoustic and optical-coherence microscope. SLD: superluminescent diode. Solid lines represent single-mode optical fibers. Arrowhead solid lines show data flow. Arrowhead dashed lines show the flow of system control signals.

Fig. 2
Fig. 2

x-y projection images of a nude mouse ear obtained by (A) OCT and (B) PAM. (C) Overlay of (A) and (B). (D) Photograph taken through an optical microscope. SG: sebaceous gland; BV: blood vessel.

Fig. 3
Fig. 3

x-z cross-sectional images of a mouse ear obtained by (A) OCT and (B) PAM. (C) Overlay of (A) and (B). ED, epidermis; CT, cartilage; SG, sebaceous gland; CP, capillary.

Fig. 4
Fig. 4

3D visualization of a mouse ear. (A) PAM image of the microvasculature only; (B) Dual-modality image showing the skin surface, a top view; (C) Dual-modality image showing the microvasculature in the ventral skin layer, a top view from 88 µm below the skin surface; (D) Dual-modality image showing the microvasculature in the dorsal skin layer, a top view from 148 µm below the skin surface. The bounding box has dimensions of 3.6 mm x 3.6 mm x 0.4 mm.

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