Abstract

Photoacoustic microscopy was developed to achieve volumetric imaging of the anatomy and functions of the subcutaneous microvasculature in both small animals and humans in vivo with high spatial resolution and high signal-to-background ratio. By following the skin contour in raster scanning, the ultrasonic transducer maintains focusing in the region of interest. Furthermore, off-focus lateral resolution is improved by using a synthetic-aperture focusing technique based on the virtual point detector concept. Structural images are acquired in both rats and humans, whereas functional images representing hemoglobin oxygen saturation are acquired in rats. After multiscale vesselness filtering, arterioles and venules in the image are separated based on the imaged oxygen saturation levels. Detailed structural information, such as vessel depth and spatial orientation, are revealed by volume rendering.

© 2006 Optical Society of America

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2006 (3)

M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77, 041101 (2006).
[Crossref]

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

M.-L. Li, H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Improved in-vivo photoacoustic microscopy based on a virtual detector concept,” Opt. Lett. 31, 474–476 (2006).
[Crossref] [PubMed]

2005 (1)

2003 (5)

C. M. van Vemmel, L. J. Spreeuwers, M. A. Viergever, and W. J. Niessen, “Level-set-based artery-vein separation in blood pool agent CE-MR angiograms,” IEEE Trans. Med. Imaging. 22, 1224–1234 (2003).
[Crossref]

M. Xu and L. V. Wang, “Analytic explanation of spatial resolution related to bandwidth and detector aperture size in thermoacoustic and photoacoustic reconstruction,” Phys. Rev. E 67, 1–15 (2003).
[Crossref]

M. C. Pilatou, N. J. Voogd, F. F. M. de Mul, and W. Steenbergen, “Analysis of three-dimensional photoacoustic imaging of a vasculature tree in vitro,” Rev. Sci. Instrum. 74, 4495–4499 (2003).
[Crossref]

R. G. Kolkman, E. Hondebrink, W. Steenbergen, and F. F. M. de Mul, “In vivo photoacoustic imaging of blood vessels using an extreme-narrow aperture sensor,” IEEE J. Sel. Top. Quantum Electron 9, 343–346 (2003).
[Crossref]

X. Wang, Y. Pang, G. Ku, G. Stoica, and L. V. Wang, “Three-dimensional laser-induced photoacoustic tomography of mouse brain with the skin and skull intact,” Opt. Lett. 28, 1739–1741 (2003).
[Crossref] [PubMed]

2000 (2)

X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 25, 114–116 (2000).

P. Carmeliet and R. K. Jain, “Angiogenesis in cancer and other disease,” Nature 407, 249–257 (2000).
[Crossref] [PubMed]

1998 (2)

C. G. A. Hoelen, F. F. M. de Mul, R. Pongers, and A. Dekker, “Three-dimensional photoacoustic imaging of blood vessels in tissue,” Opt. Lett. 23, 648–650 (1998).
[Crossref]

H. Nakajima, T. Minabe, and N. Imanishi, “Three-dimensional analysis and classification of arteries in the skin and subcutaneous adipofascial tissue by computer graphics imaging,” Plast. Reconstr. Surg. 102, 748–760 (1998).
[Crossref] [PubMed]

1992 (1)

R. L. Barnhill, K. Fandrey, M. A. Levy, M. C. Mihm, and B. Hyman, “Angiogenesis and tumor progression of melanoma: quantification of vascularity in melanocytic nevi and cutaneous malignant melanoma,” Lab. Invest. 67, 331–337 (1992).
[PubMed]

1990 (1)

R. R. Edelman, H. P. Mattle, D. J. Atkinson, and H. M. Hoogewoud, “MR angiography,” Am. J. Roentgenol. 154, 937–946 (1990).

Atkinson, D. J.

R. R. Edelman, H. P. Mattle, D. J. Atkinson, and H. M. Hoogewoud, “MR angiography,” Am. J. Roentgenol. 154, 937–946 (1990).

Barnhill, R. L.

R. L. Barnhill, K. Fandrey, M. A. Levy, M. C. Mihm, and B. Hyman, “Angiogenesis and tumor progression of melanoma: quantification of vascularity in melanocytic nevi and cutaneous malignant melanoma,” Lab. Invest. 67, 331–337 (1992).
[PubMed]

Carmeliet, P.

P. Carmeliet and R. K. Jain, “Angiogenesis in cancer and other disease,” Nature 407, 249–257 (2000).
[Crossref] [PubMed]

Chen, Z.

Y. Zhao, Z. Chen, C. Saxer, S. Xiang, J. F. de Boer, and J. S. Nelson, “Phase-resolved optical coherence tomography and optical Doppler tomography for imaging blood flow in human skin with fast scanning speed and high velocity sensitivity,” Opt. Lett. 25, 114–116 (2000).

de Boer, J. F.

Y. Zhao, Z. Chen, C. Saxer, S. Xiang, J. F. de Boer, and J. S. Nelson, “Phase-resolved optical coherence tomography and optical Doppler tomography for imaging blood flow in human skin with fast scanning speed and high velocity sensitivity,” Opt. Lett. 25, 114–116 (2000).

de Mul, F. F. M.

M. C. Pilatou, N. J. Voogd, F. F. M. de Mul, and W. Steenbergen, “Analysis of three-dimensional photoacoustic imaging of a vasculature tree in vitro,” Rev. Sci. Instrum. 74, 4495–4499 (2003).
[Crossref]

R. G. Kolkman, E. Hondebrink, W. Steenbergen, and F. F. M. de Mul, “In vivo photoacoustic imaging of blood vessels using an extreme-narrow aperture sensor,” IEEE J. Sel. Top. Quantum Electron 9, 343–346 (2003).
[Crossref]

C. G. A. Hoelen, F. F. M. de Mul, R. Pongers, and A. Dekker, “Three-dimensional photoacoustic imaging of blood vessels in tissue,” Opt. Lett. 23, 648–650 (1998).
[Crossref]

Dekker, A.

Duck, F. A.

F. A. Duck, Physical Properties of Tissue (Academic Press, San Diego, CA, 1990).

Edelman, R. R.

R. R. Edelman, H. P. Mattle, D. J. Atkinson, and H. M. Hoogewoud, “MR angiography,” Am. J. Roentgenol. 154, 937–946 (1990).

Fandrey, K.

R. L. Barnhill, K. Fandrey, M. A. Levy, M. C. Mihm, and B. Hyman, “Angiogenesis and tumor progression of melanoma: quantification of vascularity in melanocytic nevi and cutaneous malignant melanoma,” Lab. Invest. 67, 331–337 (1992).
[PubMed]

Frangi, A. F.

A. F. Frangi, W. J. Niessen, K. L. Vincken, and M. A. Viergever, “Multiscale vessel enhancement filtering,” in Proceedings of Medical Image Computing & Computer Assisted Intervention (MICCAI), W. Wells, A. Colchester, and S. Delp, eds., Vol. 1496 of Lecture Notes in Computer Science, (Springer-Verlag, Berlin1998), pp.130–137.

Hoelen, C. G. A.

Hondebrink, E.

R. G. Kolkman, E. Hondebrink, W. Steenbergen, and F. F. M. de Mul, “In vivo photoacoustic imaging of blood vessels using an extreme-narrow aperture sensor,” IEEE J. Sel. Top. Quantum Electron 9, 343–346 (2003).
[Crossref]

Hoogewoud, H. M.

R. R. Edelman, H. P. Mattle, D. J. Atkinson, and H. M. Hoogewoud, “MR angiography,” Am. J. Roentgenol. 154, 937–946 (1990).

Hyman, B.

R. L. Barnhill, K. Fandrey, M. A. Levy, M. C. Mihm, and B. Hyman, “Angiogenesis and tumor progression of melanoma: quantification of vascularity in melanocytic nevi and cutaneous malignant melanoma,” Lab. Invest. 67, 331–337 (1992).
[PubMed]

Imanishi, N.

H. Nakajima, T. Minabe, and N. Imanishi, “Three-dimensional analysis and classification of arteries in the skin and subcutaneous adipofascial tissue by computer graphics imaging,” Plast. Reconstr. Surg. 102, 748–760 (1998).
[Crossref] [PubMed]

Jain, R. K.

P. Carmeliet and R. K. Jain, “Angiogenesis in cancer and other disease,” Nature 407, 249–257 (2000).
[Crossref] [PubMed]

Jensen, D.

D. Jensen, The principles of physiology (Appleton-Century-Crofts, New York1976), pp 746.

Karabutov, A. A.

A. A. Oraevsky and A. A. Karabutov, “Optoacoustic Tomography,” in Biomedical Photonics Handbook, T. Vo-Dinh ed. (CRC Press, Boca Raton, FL, 2003).

Kolkman, R. G.

R. G. Kolkman, E. Hondebrink, W. Steenbergen, and F. F. M. de Mul, “In vivo photoacoustic imaging of blood vessels using an extreme-narrow aperture sensor,” IEEE J. Sel. Top. Quantum Electron 9, 343–346 (2003).
[Crossref]

Ku, G.

X. Wang, Y. Pang, G. Ku, G. Stoica, and L. V. Wang, “Three-dimensional laser-induced photoacoustic tomography of mouse brain with the skin and skull intact,” Opt. Lett. 28, 1739–1741 (2003).
[Crossref] [PubMed]

X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 25, 114–116 (2000).

Levy, M. A.

R. L. Barnhill, K. Fandrey, M. A. Levy, M. C. Mihm, and B. Hyman, “Angiogenesis and tumor progression of melanoma: quantification of vascularity in melanocytic nevi and cutaneous malignant melanoma,” Lab. Invest. 67, 331–337 (1992).
[PubMed]

Li, M.-L.

Maslov, K.

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

M.-L. Li, H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Improved in-vivo photoacoustic microscopy based on a virtual detector concept,” Opt. Lett. 31, 474–476 (2006).
[Crossref] [PubMed]

K. Maslov, G. Stoica, and L. V. Wang, “In vivo dark-field reflection-mode photoacoustic microscopy,” Opt. Lett. 30, 625–627 (2005).
[Crossref] [PubMed]

K. Maslov, M. Sivaramakrishnan, H. F. Zhang, G. Stoica, and L. V. Wang, “Technical considerations in quantitative blood oxygenation measurement using photoacoustic microscopy in small animal in vivo,” in Photons Plus Ultrasound: Imaging and Sensing 2006, A. A. Oraevsky and L. V. Wang, eds., Proc. SPIE6086, 215–225 (2006).

Mattle, H. P.

R. R. Edelman, H. P. Mattle, D. J. Atkinson, and H. M. Hoogewoud, “MR angiography,” Am. J. Roentgenol. 154, 937–946 (1990).

Mihm, M. C.

R. L. Barnhill, K. Fandrey, M. A. Levy, M. C. Mihm, and B. Hyman, “Angiogenesis and tumor progression of melanoma: quantification of vascularity in melanocytic nevi and cutaneous malignant melanoma,” Lab. Invest. 67, 331–337 (1992).
[PubMed]

Minabe, T.

H. Nakajima, T. Minabe, and N. Imanishi, “Three-dimensional analysis and classification of arteries in the skin and subcutaneous adipofascial tissue by computer graphics imaging,” Plast. Reconstr. Surg. 102, 748–760 (1998).
[Crossref] [PubMed]

Nakajima, H.

H. Nakajima, T. Minabe, and N. Imanishi, “Three-dimensional analysis and classification of arteries in the skin and subcutaneous adipofascial tissue by computer graphics imaging,” Plast. Reconstr. Surg. 102, 748–760 (1998).
[Crossref] [PubMed]

Nelson, J. S.

Y. Zhao, Z. Chen, C. Saxer, S. Xiang, J. F. de Boer, and J. S. Nelson, “Phase-resolved optical coherence tomography and optical Doppler tomography for imaging blood flow in human skin with fast scanning speed and high velocity sensitivity,” Opt. Lett. 25, 114–116 (2000).

Niessen, W. J.

C. M. van Vemmel, L. J. Spreeuwers, M. A. Viergever, and W. J. Niessen, “Level-set-based artery-vein separation in blood pool agent CE-MR angiograms,” IEEE Trans. Med. Imaging. 22, 1224–1234 (2003).
[Crossref]

A. F. Frangi, W. J. Niessen, K. L. Vincken, and M. A. Viergever, “Multiscale vessel enhancement filtering,” in Proceedings of Medical Image Computing & Computer Assisted Intervention (MICCAI), W. Wells, A. Colchester, and S. Delp, eds., Vol. 1496 of Lecture Notes in Computer Science, (Springer-Verlag, Berlin1998), pp.130–137.

Oraevsky, A. A.

A. A. Oraevsky and A. A. Karabutov, “Optoacoustic Tomography,” in Biomedical Photonics Handbook, T. Vo-Dinh ed. (CRC Press, Boca Raton, FL, 2003).

Pang, Y.

X. Wang, Y. Pang, G. Ku, G. Stoica, and L. V. Wang, “Three-dimensional laser-induced photoacoustic tomography of mouse brain with the skin and skull intact,” Opt. Lett. 28, 1739–1741 (2003).
[Crossref] [PubMed]

X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 25, 114–116 (2000).

Pilatou, M. C.

M. C. Pilatou, N. J. Voogd, F. F. M. de Mul, and W. Steenbergen, “Analysis of three-dimensional photoacoustic imaging of a vasculature tree in vitro,” Rev. Sci. Instrum. 74, 4495–4499 (2003).
[Crossref]

Pongers, R.

Saxer, C.

Y. Zhao, Z. Chen, C. Saxer, S. Xiang, J. F. de Boer, and J. S. Nelson, “Phase-resolved optical coherence tomography and optical Doppler tomography for imaging blood flow in human skin with fast scanning speed and high velocity sensitivity,” Opt. Lett. 25, 114–116 (2000).

Sivaramakrishnan, M.

K. Maslov, M. Sivaramakrishnan, H. F. Zhang, G. Stoica, and L. V. Wang, “Technical considerations in quantitative blood oxygenation measurement using photoacoustic microscopy in small animal in vivo,” in Photons Plus Ultrasound: Imaging and Sensing 2006, A. A. Oraevsky and L. V. Wang, eds., Proc. SPIE6086, 215–225 (2006).

Spreeuwers, L. J.

C. M. van Vemmel, L. J. Spreeuwers, M. A. Viergever, and W. J. Niessen, “Level-set-based artery-vein separation in blood pool agent CE-MR angiograms,” IEEE Trans. Med. Imaging. 22, 1224–1234 (2003).
[Crossref]

Steenbergen, W.

R. G. Kolkman, E. Hondebrink, W. Steenbergen, and F. F. M. de Mul, “In vivo photoacoustic imaging of blood vessels using an extreme-narrow aperture sensor,” IEEE J. Sel. Top. Quantum Electron 9, 343–346 (2003).
[Crossref]

M. C. Pilatou, N. J. Voogd, F. F. M. de Mul, and W. Steenbergen, “Analysis of three-dimensional photoacoustic imaging of a vasculature tree in vitro,” Rev. Sci. Instrum. 74, 4495–4499 (2003).
[Crossref]

Stoica, G.

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

M.-L. Li, H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Improved in-vivo photoacoustic microscopy based on a virtual detector concept,” Opt. Lett. 31, 474–476 (2006).
[Crossref] [PubMed]

K. Maslov, G. Stoica, and L. V. Wang, “In vivo dark-field reflection-mode photoacoustic microscopy,” Opt. Lett. 30, 625–627 (2005).
[Crossref] [PubMed]

X. Wang, Y. Pang, G. Ku, G. Stoica, and L. V. Wang, “Three-dimensional laser-induced photoacoustic tomography of mouse brain with the skin and skull intact,” Opt. Lett. 28, 1739–1741 (2003).
[Crossref] [PubMed]

X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 25, 114–116 (2000).

K. Maslov, M. Sivaramakrishnan, H. F. Zhang, G. Stoica, and L. V. Wang, “Technical considerations in quantitative blood oxygenation measurement using photoacoustic microscopy in small animal in vivo,” in Photons Plus Ultrasound: Imaging and Sensing 2006, A. A. Oraevsky and L. V. Wang, eds., Proc. SPIE6086, 215–225 (2006).

van Vemmel, C. M.

C. M. van Vemmel, L. J. Spreeuwers, M. A. Viergever, and W. J. Niessen, “Level-set-based artery-vein separation in blood pool agent CE-MR angiograms,” IEEE Trans. Med. Imaging. 22, 1224–1234 (2003).
[Crossref]

Viergever, M. A.

C. M. van Vemmel, L. J. Spreeuwers, M. A. Viergever, and W. J. Niessen, “Level-set-based artery-vein separation in blood pool agent CE-MR angiograms,” IEEE Trans. Med. Imaging. 22, 1224–1234 (2003).
[Crossref]

A. F. Frangi, W. J. Niessen, K. L. Vincken, and M. A. Viergever, “Multiscale vessel enhancement filtering,” in Proceedings of Medical Image Computing & Computer Assisted Intervention (MICCAI), W. Wells, A. Colchester, and S. Delp, eds., Vol. 1496 of Lecture Notes in Computer Science, (Springer-Verlag, Berlin1998), pp.130–137.

Vincken, K. L.

A. F. Frangi, W. J. Niessen, K. L. Vincken, and M. A. Viergever, “Multiscale vessel enhancement filtering,” in Proceedings of Medical Image Computing & Computer Assisted Intervention (MICCAI), W. Wells, A. Colchester, and S. Delp, eds., Vol. 1496 of Lecture Notes in Computer Science, (Springer-Verlag, Berlin1998), pp.130–137.

Voogd, N. J.

M. C. Pilatou, N. J. Voogd, F. F. M. de Mul, and W. Steenbergen, “Analysis of three-dimensional photoacoustic imaging of a vasculature tree in vitro,” Rev. Sci. Instrum. 74, 4495–4499 (2003).
[Crossref]

Wang, L. V.

M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77, 041101 (2006).
[Crossref]

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

M.-L. Li, H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Improved in-vivo photoacoustic microscopy based on a virtual detector concept,” Opt. Lett. 31, 474–476 (2006).
[Crossref] [PubMed]

K. Maslov, G. Stoica, and L. V. Wang, “In vivo dark-field reflection-mode photoacoustic microscopy,” Opt. Lett. 30, 625–627 (2005).
[Crossref] [PubMed]

X. Wang, Y. Pang, G. Ku, G. Stoica, and L. V. Wang, “Three-dimensional laser-induced photoacoustic tomography of mouse brain with the skin and skull intact,” Opt. Lett. 28, 1739–1741 (2003).
[Crossref] [PubMed]

M. Xu and L. V. Wang, “Analytic explanation of spatial resolution related to bandwidth and detector aperture size in thermoacoustic and photoacoustic reconstruction,” Phys. Rev. E 67, 1–15 (2003).
[Crossref]

X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 25, 114–116 (2000).

K. Maslov, M. Sivaramakrishnan, H. F. Zhang, G. Stoica, and L. V. Wang, “Technical considerations in quantitative blood oxygenation measurement using photoacoustic microscopy in small animal in vivo,” in Photons Plus Ultrasound: Imaging and Sensing 2006, A. A. Oraevsky and L. V. Wang, eds., Proc. SPIE6086, 215–225 (2006).

Wang, X.

X. Wang, Y. Pang, G. Ku, G. Stoica, and L. V. Wang, “Three-dimensional laser-induced photoacoustic tomography of mouse brain with the skin and skull intact,” Opt. Lett. 28, 1739–1741 (2003).
[Crossref] [PubMed]

X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 25, 114–116 (2000).

Xiang, S.

Y. Zhao, Z. Chen, C. Saxer, S. Xiang, J. F. de Boer, and J. S. Nelson, “Phase-resolved optical coherence tomography and optical Doppler tomography for imaging blood flow in human skin with fast scanning speed and high velocity sensitivity,” Opt. Lett. 25, 114–116 (2000).

Xie, X.

X. Wang, Y. Pang, G. Ku, X. Xie, G. Stoica, and L. V. Wang, “Noninvasive laser-induced photoacoustic tomography for structural and functional in vivo imaging of the brain,” Nat. Biotechnol. 25, 114–116 (2000).

Xu, M.

M. Xu and L. V. Wang, “Photoacoustic imaging in biomedicine,” Rev. Sci. Instrum. 77, 041101 (2006).
[Crossref]

M. Xu and L. V. Wang, “Analytic explanation of spatial resolution related to bandwidth and detector aperture size in thermoacoustic and photoacoustic reconstruction,” Phys. Rev. E 67, 1–15 (2003).
[Crossref]

Zhang, H. F.

M.-L. Li, H. F. Zhang, K. Maslov, G. Stoica, and L. V. Wang, “Improved in-vivo photoacoustic microscopy based on a virtual detector concept,” Opt. Lett. 31, 474–476 (2006).
[Crossref] [PubMed]

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

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Figures (4)

Fig. 1.
Fig. 1.

Schematic of the PAM system.

Fig 2.
Fig 2.

Structural imaging of the subcutaneous microvasculature in rats in vivo. (A) An MAP image. (B) (1.6 MB) A movie of the volume-rendered microvasculature viewed from different angles.

Fig. 3.
Fig. 3.

(2.2 MB) A movie showing in vivo functional images representing SO2 in single blood vessels of rats. Venules and arterioles are colored blue and red, respectively. The imaged average SO2 values in the arterioles and venoules were 0.99±0.01 and 0.81±0.02, respectively.

Fig. 4.
Fig. 4.

Volumetric imaging of the subcutaneous blood vessels in the palm of a human hand in vivo.

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