volume | PIER Journals

Abstract

Photoacoustic tomography (PAT) is an emerging imaging modality that shows great potential for preclinical research and clinical practice. As a hybrid technique, PAT is based on the acoustic detection of optical absorption from either endogenous chromophores, such as oxy-hemoglobin and deoxy-hemoglobin, or exogenous contrast agents, such as organic dyes and nanoparticles. Because ultrasound scatters much less than light in tissue, PAT generates high-resolution images in both the optical ballistic and diffusive regimes. Over the past decade, the photoacoustic technique has been evolving rapidly, leading to a variety of exciting discoveries and applications. This review covers the basic principles of PAT and its different implementations. Strengths of PAT are highlighted, along with the most recent imaging results.

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29. Nasiriavanaki, M., J. Xia, H. Wan, A. Q. Bauer, J. P. Culver, and L. V. Wang, "High-resolution photoacoustic tomography of resting-state functional connectivity in the mouse brain," Proc. Natl. Acad. Sci. USA, Vol. 111, 21-26, Jan. 7, 2014.

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36. Favazza, C. P., L. A. Cornelius, and L. H. V. Wang, "In vivo functional photoacoustic microscopy of cutaneous microvasculature in human skin," Journal of Biomedical Optics, Vol. 16, 026004, Feb. 2011.

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38. Song, L. A., K. Maslov, K. K. Shung, and L. H. V. Wang, "Ultrasound-array-based real-time photoacoustic microscopy of human pulsatile dynamics in vivo," Journal of Biomedical Optics, Vol. 15, 021303, Mar.-Apr. 2010.

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40. Rowland, K. J., J. J. Yao, L. D. Wang, C. R. Erwin, K. I. Maslov, L. H. V. Wang, and B. W.Warner, "Immediate alterations in intestinal oxygen saturation and blood fow after massive small bowel resection as measured by photoacoustic microscopy," Journal of Pediatric Surgery,, Vol. 47, 1143-1149, Jun. 2012.

41. Yao, J., K. I. Maslov, E. R. Puckett, K. J. Rowland, B. W. Warner, and L. V. Wang, "Double-illumination photoacoustic microscopy," Optics Letters, Vol. 37, 659-661, 2012.

42. Yang, J.-M., R. Chen, C. Favazza, J. Yao, Q. Zhou, K. K. Shung, and L. V. Wang, "A 2.5-mm outer diameter photoacoustic endoscopic mini-probe based on a highly sensitive PMN-PT ultrasonic transducer," Photons Plus Ultrasound: Imaging and Sensing 2012, 82233M-82233M-6, San Francisco, California, USA, 2012.

43. Yang, J.-M., C. Favazza, R. Chen, J. Yao, X. Cai, K. Maslov, Q. Zhou, K. K. Shung, and L. V. Wang, "Toward dual-wavelength functional photoacoustic endoscopy: Laser and peripheral optical systems development," Photons Plus Ultrasound: Imaging and Sensing 2012, 822316-822316-7, San Francisco, California, USA, 2012.

44. Yao, J., K. J. Rowland, L. Wang, K. I. Maslov, B. W. Warner, and L. V. Wang, "Double-illumination photoacoustic microscopy of intestinal hemodynamics following massive small bowel resection," Photons Plus Ultrasound: Imaging and Sensing 2012, 82233V-82233V-7, San Francisco, California, USA, 2012.

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49. Maslov, K. and L. V. Wang, "Photoacoustic imaging of biological tissue with intensity-modulated continuous-wave laser," Journal of Biomedical Optics, Vol. 13, 024006, 2008.

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52. Paproski, R. J., A. E. Forbrich, K. Wachowicz, M. M. Hitt, and R. J. Zemp, "Tyrosinase as a dual reporter gene for both photoacoustic and magnetic resonance imaging," Biomedical Optics Express, Vol. 2, 771-780, Apr. 1, 2011.

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55. Pramanik, M. and L. V. Wang, "Thermoacoustic and photoacoustic sensing of temperature," Journal of Biomedical Optics, Vol. 14, 054024, Sep.-Oct. 2009.

56. Wang, L., J. Xia, J. Yao, K. I. Maslov, and L. V. Wang, "Ultrasonically encoded photoacoustic flowgraphy in biological tissue," Physical Review Letters, Vol. 111, 204301, 2013.

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61. Xu, Y. and L. V. Wang, "Time reversal and its application to tomography with diffracting sources," Physical Review Letters, Vol. 92, 033902, 2004.

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63. Yulia, H., K. Peter, and N. Linh, "Reconstruction and time reversal in thermoacoustic tomography in acoustically homogeneous and inhomogeneous media," Inverse Problems, Vol. 24, 055006, 2008.

64. Treeby, B. E. and B. T. Cox, "k-Wave: MATLAB toolbox for the simulation and reconstruction of photoacoustic wave fields," Journal of Biomedical Optics, Vol. 15, 021314, Mar.-Apr. 2010.

65. Xu, M. H. and L. V. Wang, "Analytic explanation of spatial resolution related to bandwidth and detector aperture size in thermoacoustic or photoacoustic reconstruction," Physical Review E, Vol. 67, 15, May 2003.

66. Wang, K., R. Su, A. A. Oraevsky, and M. A. Anastasio, "Investigation of iterative image reconstruction in three-dimensional optoacoustic tomography," Physics in Medicine and Biology, Vol. 57, 5399-5423, Sep. 2012.

67. Wang, K., S. A. Ermilov, R. Su, H. P. Brecht, A. A. Oraevsky, and M. A. Anastasio, "An imaging model incorporating ultrasonic transducer properties for three-dimensional optoacoustic tomography," IEEE Transactions on Medical Imaging, Vol. 30, 203-214, Feb. 2011.

68. Xu, Y., L. V. Wang, G. Ambartsoumian, and P. Kuchment, "Reconstructions in limited-view thermoacoustic tomography," Medical Physics, Vol. 31, 724-733, Apr. 2004.

69. Guo, Z., C. Li, L. Song, and L. V. Wang, "Compressed sensing in photoacoustic tomography in vivo," Journal of Biomedical Optics, Vol. 15, 021311, 2010.

70. Huang, B., J. Xia, K. Maslov, and L. V.Wang, "Improving limited-view photoacoustic tomography with an acoustic reflector," Journal of Biomedical Optics, Vol. 18, 110505, 2013.

71. Provost, J. and F. Lesage, "The application of compressed sensing for photo-acoustic tomography," IEEE Transactions on Medical Imaging, Vol. 28, 585-594, Apr. 2009.

72. Wang, Y., T. N. Erpelding, L. Jankovic, Z. Guo, J.-L. Robert, G. David, and L. V. Wang, "In vivo three-dimensional photoacoustic imaging based on a clinical matrix array ultrasound probe," Journal of Biomedical Optics, Vol. 17, 061208-1, 2012.

73. Zhang, E., J. Laufer, and P. Beard, "Backward-mode multiwavelength photoacoustic scanner using a planar Fabry-Perot polymer film ultrasound sensor for high-resolution three-dimensional imaging of biological tissues," Appl. Opt., Vol. 47, 561-577, 2008.

74. Laufer, J., E. Zhang, G. Raivich, and P. Beard, "Three-dimensional noninvasive imaging of the vasculature in the mouse brain using a high resolution photoacoustic scanner," Appl. Opt., Vol. 48, D299-D306, 2009.

75. Laufer, J., F. Norris, J. Cleary, E. Zhang, B. Treeby, B. Cox, P. Johnson, P. Scambler, M. Lythgoe, and P. Beard, "In vivo photoacoustic imaging of mouse embryos," Journal of Biomedical Optics, Vol. 17, 061220-1, 2012.

76. Xia, J., Z. Guo, K. Maslov, A. Aguirre, Q. Zhu, C. Percival, and L. V. Wang, "Three-dimensional photoacoustic tomography based on the focal-line concept," Journal of Biomedical Optics, Vol. 16, 090505, 2011.

77. Buehler, A., E. Herzog, D. Razansky, and V. Ntziachristos, "Video rate optoacoustic tomography of mouse kidney perfusion," Opt. Lett.,, Vol. 35, 2475-2477, 2010.

78. Xia, J., M. Chatni, K. Maslov, Z. Guo, K. Wang, M. Anastasio, and L. V. Wang, "Whole-body ring-shaped confocal photoacoustic computed tomography of small animals in vivo," Journal of Biomedical Optics, Vol. 17, 050506, 2012.

79. Xia, J., W. Chen, K. Maslov, M. A. Anastasio, and L. V. Wang, "Retrospective respiration-gated whole-body photoacoustic computed tomography of mice," Journal of Biomedical Optics, Vol. 19, 016003, 2014.

80. Kruger, R. A., W. L. Kiser, D. R. Reinecke, G. A. Kruger, and K. D. Miller, "Thermoacoustic molecular imaging of small animals," Molecular Imaging, Vol. 2, 113-123, 2003.

81. Brecht, H.-P., R. Su, M. Fronheiser, S. A. Ermilov, A. Conjusteau, and A. A. Oraevsky, "Whole-body three-dimensional optoacoustic tomography system for small animals," Journal of Biomedical Optics, Vol. 14, 064007-8, 2009.

82. Kruger, R., D. Reinecke, G. Kruger, M. Thornton, P. Picot, T. Morgan, K. Stantz, and C. Mistretta, "HYPR-spectral photoacoustic CT for preclinical imaging," Proceedings of SPIE, Vol. 7177, 71770F, 2009.

83. Kruger, R. A., C. M. Kuzmiak, R. B. Lam, D. R. Reinecke, S. P. Del Rio, and D. Steed, "Dedicated 3D photoacoustic breast imaging," Medical Physics, Vol. 40, No. 11, 113301, 2013.

84. Xu, M., "Analysis of spatial resolution in photoacoustic tomography," Photoacoustic Imaging and Spectroscopy, 47-60, CRC Press, 2009.

85. Yao, J. J. and L. H. V. Wang, "Photoacoustic microscopy," Laser & Photonics Reviews, Vol. 7, 758-778, Sep. 2013.

86. Hu, S., K. Maslov, and L. V. Wang, "Second-generation optical-resolution photoacoustic microscopy with improved sensitivity and speed," Optics Letters, Vol. 36, 1134-1136, Apr. 1, 2011.

87. Maslov, K., H. F. Zhang, S. Hu, and L. V. Wang, "Optical-resolution photoacoustic microscopy for in vivo imaging of single capillaries," Optics Letters, Vol. 33, 929-931, May 1, 2008.

88. Maslov, K., G. Stoica, and L. H. V. Wang, "In vivo dark-field reflection-mode photoacoustic microscopy," Optics Letters, Vol. 30, 625-627, Mar. 15, 2005.

89. Yang, J. M., C. Favazza, R. M. Chen, J. J. Yao, X. Cai, K. Maslov, Q. F. Zhou, K. K. Shung, and L. H. V. Wang, "Simultaneous functional photoacoustic and ultrasonic endoscopy of internal organs in vivo," Nature Medicine, Vol. 18, 1297, Aug. 2012.

90. Hajireza, P., W. Shi, and R. Zemp, "Label-free in vivo GRIN-lens optical resolution photoacoustic micro-endoscopy," Laser Physics Letters, Vol. 10, No. 5, 055603, May 2013.

91. Yang, J. M., R. M. Chen, C. Favazza, J. J. Yao, C. Y. Li, Z. L. Hu, Q. F. Zhou, K. K. Shung, and L. V. Wang, "A 2.5-mm diameter probe for photoacoustic and ultrasonic endoscopy," Optics Express, Vol. 20, 23944-23953, Oct. 8, 2012.

92. Shao, P., W. Shi, P. Hajireza, and R. J. Zemp, "Integrated micro-endoscopy system for simultaneous fluorescence and optical-resolution photoacoustic imaging," Journal of Biomedical Optics, Vol. 17, 076024, Jul. 2012.

93. Yang, J. M., K. Maslov, H. C. Yang, Q. F. Zhou, K. K. Shung, and L. H. V. Wang, "Photoacoustic endoscopy," Optics Letters, Vol. 34, 1591-1593, May 15, 2009.

94. Xing, W. X., L. D. Wang, K. Maslov, and L. H. V. Wang, "Integrated optical- and acoustic-resolution photoacoustic microscopy based on an optical fiber bundle," Optics Letters, Vol. 38, 52-54, Jan. 1, 2013.

95. Xu, X., H. Liu, and L. V. Wang, "Time-reversed ultrasonically encoded optical focusing into scattering media," Nat. Photon., Vol. 5, 154-157, 2011.

96. Judkewitz, B., Y. M. Wang, R. Horstmeyer, A. Mathy, and C. Yang, "Speckle-scale focusing in the diffusive regime with time reversal of variance-encoded light (TROVE)," Nat. Photon., Vol. 7, 300-305, 2013.

97. Li, L., R. J. Zemp, G. Lungu, G. Stoica, and L. V. Wang, "Photoacoustic imaging of lacZ gene expression in vivo," Journal of Biomedical Optics, Vol. 12, 020504-3, 2007.

98. Kruger, A., V. Schirrmacher, and R. Khokha, "The bacterial lacZ gene: An important tool for metastasis research and evaluation if new cancer therapies," Cancer and Metastasis Reviews, Vol. 17, 285-294, Sep. 1, 1998.

99. Cai, X., L. Li, A. Krumholz, Z. J. Guo, T. N. Erpelding, C. Zhang, Y. Zhang, Y. N. Xi, and L. H. V. Wang, "Multi-scale molecular photoacoustic tomography of gene expression," PLOS ONE, Vol. 7, No. 8, e43999, Aug. 27, 2012.

100. Xia, J., G. Li, L. Wang, M. Nasiriavanaki, K. Maslov, J. A. Engelbach, J. R. Garbow, and L. V. Wang, "Wide-field two-dimensional multifocal optical-resolution photoacoustic-computed microscopy," Optics Letters, Vol. 38, 5236-5239, Dec. 15, 2013.

101. Huang, B., M. Bates, and X. W. Zhuang, "Super-resolution fluorescence microscopy," Annual Review of Biochemistry, Vol. 78, 993-1016, 2009.

102. Yao, J., L. Wang, C. Li, C. Zhang, and L. V. Wang, "Photoimprint photoacoustic microscopy for three-dimensional label-free subdiffraction imaging," Physical Review Letters, Vol. 112, 014302, 2014.

103. Nedosekin, D. A., E. I. Galanzha, E. Dervishi, A. S. Biris, and V. P. Zharov, "Super-resolution nonlinear photothermal microscopy," Small, Vol. 10, 135-142, Jan. 15, 2014.

104. Conkey, D. B., A. M. Caravaca-Aguirre, J. D. Dove, H. Ju, T. W. Murray, and R. Piestun, "Super-resolution photoacoustic imaging through a scattering wall,", arXiv:1310.5736, 2013.

105. Lai, P., L. Wang, J. W. Tay, and L. Wang, "Nonlinear photoacoustic wavefront shaping (PAWS) for single speckle-grain optical focusing in scattering media,", arXiv:1402.0816, 2014.

106. Hanahan, D. and R. A. Weinberg, "Hallmarks of cancer: The next generation," Cell, Vol. 144, 646-674, Mar. 4, 2011.

107. Zhang, H. F., K. Maslov, M. Sivaramakrishnan, G. Stoica, and L. H. V. Wang, "Imaging of hemoglobin oxygen saturation variations in single vessels in vivo using photoacoustic microscopy," Applied Physics Letters, Vol. 90, 053901, Jan. 29, 2007.

108. Maslov, K., H. F. Zhang, and L. V. Wang, "Effects of wavelength-dependent fluence attenuation on the noninvasive photoacoustic imaging of hemoglobin oxygen saturation in subcutaneous vasculature in vivo," Inverse Problems, Vol. 23, S113-S122, Dec. 2007.

109. Hu, S., K. Maslov, and L. H. V. Wang, "Noninvasive label-free imaging of microhemodynamics by optical-resolution photoacoustic microscopy," Optics Express, Vol. 17, 7688-7693, Apr. 27, 2009.

110. Hu, S., K. Maslov, and L. H. V. Wang, "In vivo functional chronic imaging of a small animal model using optical-resolution photoacoustic microscopy," Medical Physics, Vol. 36, 2320-2323, Jun. 2009.

111. Hu, S., B. Rao, K. Maslov, and L. V. Wang, "Label-free photoacoustic ophthalmic angiography," Optics Letters, Vol. 35, 1-3, Jan. 1, 2010.

112. Wang, Y., K. Maslov, and L. H. V. Wang, "Spectrally encoded photoacoustic microscopy using a digital mirror device," Journal of Biomedical Optics, Vol. 17, 066020, Jun. 2012.

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Dr. Jun Xia

Dr. Junjie Yao

Dr. Lihong V. Wang