Photoacoustic viscoelasticity imaging dedicated to mechanical characterization of biological tissues

Yujiao Shi; Fen Yang; Qian Wang

doi:10.1142/s1793545817300051

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

[2] L. V. Wang, S. Hu, “Photoacoustic tomography: In vivo imaging from organelles to organs,” Science 335, 1458–1462 (2012).

[3] J. Zhang, S. Yang, X. Ji, Q. Zhou, D. Xing, “Characterization of lipid-rich aortic plaques by intravascular photoacoustic tomography,” J. Am. Coll. Cardiol. 64, 385–390 (2014).

[4] P. C. Li, C. R. C. Wang, D. B. Shieh, C. W. Wei, C. K. Liao, C. Poe, S. Jhan, A.-A. Ding, Y. N. Wu, “ In vivo photoacoustic molecular imaging with simultaneous multiple selective targeting using antibody-conjugated gold nanorods,” Opt. Express 16, 18605–18615 (2008).

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

[6] S. Yang, D. Xing, Q. Zhou, L. Xiang, Y. Lao, “ Functional imaging of cerebrovascular activities in small animals using high-resolution photoacoustic tomography,” Med. Phys. 34, 3294–3301 (2007).

[7] A. De La Zerda, C. Zavaleta, S. Keren, S. Vaithilingam, S. Bodapati, Z. Liu, J. Levi, B. R. Smith, T.-J. Ma, O. Oralkan, Z. Cheng, X. Chen, H. Dai, B. T. Khuri-Yakub, S. S. Gambhir, “ Carbon nanotubes as photoacoustic molecular imaging agents in living mice,” Nat. Nanotechnol. 3, 557–562 (2008).

[8] R. A. Kruger, P. Liu, Y. Fang, C. R. Appledorn, “ Photoacoustic ultrasound (PAUS) — reconstruction tomography,” Med. Phys. 22, 1605–1609 (1995).

[9] L. Zeng, D. Xing, H. Gu, D. Yang, S. Yang, L. Xiang, “ High antinoise photoacoustic tomography based on a modified filtered backprojection algorithm with combination wavelet,” Med. Phys. 34, 556–563 (2007).

[10] Y. Lao, D. Xing, S. Yang, L. Xiang, “ Noninvasive photoacoustic imaging of the developing vasculature during early tumor growth,” Phys. Med. Biol. 53, 4203–4212 (2008).

[11] J. W. Kim, E. I. Galanzha, E. V. Shashkov, H. M. Moon, V. P. Zharov, “ Golden carbon nanotubes as multimodal photoacoustic and photothermal high-contrast molecular agents,” Nat. Nanotechnol. 4, 688–694 (2009).

[12] L. Xiang, Y. Yuan, D. Xing, Z. Ou, S. Yang, F. Zhou, “ Photoacoustic molecular imaging with antibody-functionalized single-walled carbon nanotubes for early diagnosis of tumor,” J. Biomed. Opt. 14, 021008 (2009).

[13] C. Li, L. V. Wang, “ Photoacoustic tomography and sensing in biomedicine,” Phys. Med. Biol. 54, R59–R97 (2009).

[14] G. Huang, S. Yang, Y. Yuan, D. Xing, “ Combining X-ray and photoacoustics for in vivo tumor imaging with gold nanorods,” Appl. Phys. Lett. 99, 123701 (2011).

[15] Z. Chen, S. Yang, D. Xing, “In vivo detection of hemoglobin oxygen saturation and carboxyhemoglobin saturation with multiwavelength photoacoustic microscopy,” Opt. Lett. 37, 3414–3416 (2012).

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

[17] S. Yang, F. Ye, D. Xing, “Intracellular label-free gold nanorods imaging with photoacoustic microscopy,” Opt. Express 20, 10370–10375 (2012).

[18] B. Li, H. Qin, S. Yang, D. Xing, “ In vivo fast variable focus photoacoustic microscopy using an electrically tunable lens,” Opt. Express 22, 20130–20137 (2014).

[19] Y. S. Chen, W. Frey, S. Kim, P. Kruizinga, K. Homan, S. Emelianov, “Silica-coated gold nanorods as photoacoustic signal nanoamplifiers,” Nano Lett. 11, 348–354 (2011).

[20] X. Ji, K. Xiong, S. Yang, D. Xing, “Intravascular confocal photoacoustic endoscope with dual-element ultrasonic transducer,” Opt. Express 23, 9130–9136 (2015).

[21] G. He, D. Xu, H. Qin, S. Yang, D. Xing, “ In vivo cell characteristic extraction and identification by photoacoustic flow cytography,” Biomed. Opt. Express 6, 3748–3756 (2015).

[22] L. Song, K. Maslov, R. Bitton, K. K. Shung, L. V. Wang, “Fast 3-D dark-field reflection-mode photoacoustic microscopy in vivo with a 30-MHz ultrasound linear array,” J. Biomed. Opt. 13, 054028 (2008).

[23] Y. Shi, H. Qin, S. Yang, D. Xing, “Thermally confined shell coating amplifies the photoacoustic conversion efficiency of nanoprobes,” Nano Res. 9, 3644–3655 (2016).

[24] Z. Chen, S. Yang, Y. Wang, D. Xing, “Noncontact broadband all-optical photoacoustic microscopy based on a low-coherence interferometer,” Appl. Phys. Lett. 106, 043701 (2015).

[25] E. Z. Zhang, J. G. Laufer, R. B. Pedley, P. C. Beard, “ In vivo high-resolution 3D photoacoustic imaging of superficial vascular anatomy,” Phys. Med. Biol. 54, 1035–1046 (2009).

[26] Y. Wang, D. Xu, S. Yang, D. Xing, “ Toward in vivo biopsy of melanoma based on photoacoustic and ultrasound dual imaging with an integrated detector,” Biomed. Opt. Express 7, 279–286 (2016).

[27] Y. Liu, X. Yang, D. Zhu, R. Shi, Q. Luo, “ Optical clearing agents improve photoacoustic imaging in the optical diffusive regime,” Opt. Lett. 38, 4236–4239 (2013).

[28] D. Xu, S. Yang, Y. Wang, Y. Gu, D. Xing, “ Noninvasive and high-resolving photoacoustic dermoscopy of human skin,” Biomed. Opt. Express 7, 2095–2102 (2016).

[29] Z. Chen, S. Yang, D. Xing, “ Optically integrated trimodality imaging system: Combined all-optical photoacoustic microscopy, optical coherence tomography, and fluorescence imaging,” Opt. Lett. 41, 1636–1639 (2016).

[30] S. Mallidi, T. Larson, J. Tam, P. P. Joshi, A. Karpiouk, K. Sokolov, S. Emelianov, “ Multiwavelength photoacoustic imaging and plasmon resonance coupling of gold nanoparticles for selective detection of cancer,” Nano Lett. 9, 2825–2831 (2009).

[31] J. Zhong, S. Yang, L. Wen, D. Xing, “ Imaging-guided photoacoustic drug release and synergistic chemo-photoacoustic therapy with paclitaxel-containing nanoparticles,” J. Control. Release 226, 77–87 (2016).

[32] H. Qin, T. Zhou, S. Yang, D. Xing, “ Fluorescence quenching nanoprobes dedicated to in vivo photoacoustic imaging and high-efficient tumor therapy in deep-seated tissue,” Small 11, 2675–2686 (2015).

[33] J. Shah, S. Park, S. Aglyamov, T. Larson, L. Ma, K. Sokolov, K. Johnston, T. Milner, S. Y. Emelianov, “ Photoacoustic imaging and temperature measurement for photothermal cancer therapy,” J. Biomed. Opt. 13, 034024 (2008).

[34] A. G. Bell, “ On the production and reproduction of sound by light,” Am. J. Sci. 118, 305–324 (1880).

[35] G. J. Diebold, T. Sun, M. I. Khan, “ Photoacoustic monopole radiation in one, two, and three dimensions,” Phys. Rev. Lett. 67, 3384–3387 (1991).

[36] A. Rosencwaig, A. Gersho, “ Theory of the photoacoustic effect with solids,” J. Appl. Phys. 47, 64–69 (1976).

[37] C. Lou, S. Yang, Z. Ji, Q. Chen, D. Xing, “ Ultrashort microwave-induced thermoacoustic imaging: A breakthrough in excitation efficiency and spatial resolution,” Phys. Rev. Lett. 109, 218101 (2012).

[38] Z. Ji, W. Ding, F. Ye, C. Lou, D. Xing, “ Shape-adapting thermoacoustic imaging system based on flexible multi-element transducer,” Appl. Phys. Lett. 107, 094104 (2015).

[39] J. F. Greenleaf, M. Fatemi, M. Insana, “ Selected methods for imaging elastic properties of biological tissues,” Annu. Rev. Biomed. Eng. 5, 57–78 (2003).

[40] T. Xydeas, K. Siegmann, R. Sinkus, U. Krainick-Strobel, S. Miller, C. D. Claussen, “ Magnetic resonance elastography of the breast: Correlation of signal intensity data with viscoelastic properties,” Invest. Radiol. 40, 412–420 (2005).

[41] J. Rogowska, N. A. Patel, J. G. Fujimoto, M. E. Brezinski, “ Optical coherence tomographic elastography technique for measuring deformation and strain of atherosclerotic tissues,” Heart 90, 556–562 (2004).

[42] G. Gao, S. Yang, D. Xing, “ Viscoelasticity imaging of biological tissues with phase-resolved photoacoustic measurement,” Opt. Lett. 36, 3341–3343 (2011).

[43] Y. Zhao, S. Yang, C. Chen, D. Xing, “ Simultaneous optical absorption and viscoelasticity imaging based on photoacoustic lock-in measurement,” Opt. Lett. 39, 2565–2568 (2014).

[44] C. Chen, Y. Zhao, S. Yang, D. Xing, “ Mechanical characterization of intraluminal tissue with phase-resolved photoacoustic viscoelasticity endoscopy,” Biomed. Opt. Express 6, 4975–4980 (2015).

[45] C. Chen, Y. Zhao, S. Yang, D. Xing, “ Integrated mechanical and structural features for photoacoustic characterization of atherosclerosis using a quasi-continuous laser,” Opt. Express 23, 17309–17315 (2015).

[46] Y. Zhao, C. Chen, S. Yang, D. Xing, “ Mechanical evaluation of lipid accumulation in atherosclerotic tissues by photoacoustic viscoelasticity imaging,” Opt. Lett. 41, 4522–4525 (2016).

[47] Y. Zhao, C. Chen, H. Liu, S. Yang, D. Xing, “ Time-resolved photoacoustic measurement for evaluation of viscoelastic properties of biological tissues,” Appl. Phys. Lett. 109, 203702 (2016).

[48] L. B. Eldred, W. P. Baker, A. N. Palazotto, “ Kelvin–Voigt versus fractional derivative model as constitutive relations for viscoelastic materials,” AIAA J. 33, 547–550 (1995).

[49] J. Chen, R. Lin, H. Wang, J. Meng, H. Zheng, L. Song, “ Blind-deconvolution optical-resolution photoacoustic microscopy in vivo,” Opt. Express 21, 7316–7327 (2013).

[50] V. Swaminathan, K. Mythreye, E. T. O’Brien, A. Berchuck, G. C. Blobe, R. Superfine, “ Mechanical stiffness grades metastatic potential in patient tumor cells and in cancer cell lines,” Cancer Res. 71, 5075–5080 (2011).

[51] R. P. Araujo, D. L. S. McElwain, “ A linear-elastic model of anisotropic tumour growth,” Eur. J. Appl. Math. 15, 365–384 (2004).

[52] A. Lyshchik, T. Higashi, R. Asato, S. Tanaka, J. Ito, J. J. Mai, C. Pellot-Barakat, M. F. Insana, A. B. Brill, T. Saga, M. Hiraoka, K. Togashi, “ Thyroid gland tumor diagnosis at US elastography,” Radiology 237, 202–211 (2005).

[53] M. J. Paszek, N. Zahir, K. R. Johnson, J. N. Lakins, G. I. Rozenberg, A. Gefen, C. A. Reinhart-King, S. S. Margulies, M. Dembo, D. Boettiger, D. A. Hammer, V. M. Weaver, “ Tensional homeostasis and the malignant phenotype,” Cancer Cell 8, 241–254 (2005).

[54] A. J. Lusis, “ Atherosclerosis,” Nature 407, 233–241 (2000).

[55] C. K. Glass, J. L. Witztum, “ Atherosclerosis: The road ahead,” Cell 104, 503–516 (2001).

[56] R. Virmani, A. P. Burke, A. Farb, F. D. Kolodgie, “ Pathology of the vulnerable plaque,” J. Am. Coll. Cardiol. 47, C13–C18 (2006).

[57] C. L. De Korte, S. G. Carlier, F. Mastik, M. M. Doyley, A. F. W. Van Der Steen, P. W. Serruys, N. Bom, “ Morphological and mechanical information of coronary arteries obtained with intravascular elastography: Feasibility study in vivo,” Eur. Heart J. 23, 405–413 (2002).

[58] Q. Lu, K. Ganesan, D. T. Simionescu, N. R. Vyavahare, “ Novel porous aortic elastin and collagen scaffolds for tissue engineering,” Biomaterials 25, 5227–5237 (2004).

[59] L. W. Lake, C. D. Armeniades, “ Structure-property relations of aortic tissue,” ASAIO J. 18, 202–208 (1972).

[60] L. Yoo, V. Gupta, C. Lee, P. Kavehpore, J. L. Demer, “ Viscoelastic properties of bovine orbital connective tissue and fat: Constitutive models,” Biomech. Model. Mechanobiol. 10, 901–914 (2011).

[61] J. Ophir, I. Cespedes, H. Ponnenkanti, Y. Yazdi, X. Li, “ Elastography: A quantitative method for imaging the elasticity of biological tissues,” Ultrason. Imaging 13, 111–134 (1991).

[62] R. Muthupillai, D. J. Lomas, P. J. Rossman, J. F. Greenleaf, R. L. Ehman, “ Magnetic resonance elastography by direct visualization of propagating acoustic strain waves,” Science 269, 1854–1857 (1995).

[63] R. K. Wang, Z. H. Ma, S. J. Kirkpatrick, “ Tissue Doppler optical coherence elastography for real time strain rate and strain mapping of soft tissue,” Appl. Phys. Lett. 89, 144103 (2006).

[64] P. F. Hai, J. J. Yao, G. Li, C. Y. Li, L. V. Wang, “ Photoacoustic elastography,” Opt. Lett. 41, 725–728 (2016).

[65] M. Takezaki, N. Hirota, M. Terazima, “ Nonradiative relaxation processes and electronically excited states of nitrobenzene studied by picosecond time-resolved transient grating method,” J. Phys. Chem. A 101, 3443–3448 (1997).