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Quantitative Ultrasound for Nondestructive Characterization of Engineered Tissues and Biomaterials

  • Nondestructive Characterization of Biomaterials for Tissue Engineering and Drug Delivery
  • Published:
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Abstract

Non-invasive, non-destructive technologies for imaging and quantitatively monitoring the development of artificial tissues are critical for the advancement of tissue engineering. Current standard techniques for evaluating engineered tissues, including histology, biochemical assays and mechanical testing, are destructive approaches. Ultrasound is emerging as a valuable tool for imaging and quantitatively monitoring the properties of engineered tissues and biomaterials longitudinally during fabrication and post-implantation. Ultrasound techniques are rapid, non-invasive, non-destructive and can be easily integrated into sterile environments necessary for tissue engineering. Furthermore, high-frequency quantitative ultrasound techniques can enable volumetric characterization of the structural, biological, and mechanical properties of engineered tissues during fabrication and post-implantation. This review provides an overview of ultrasound imaging, quantitative ultrasound techniques, and elastography, with representative examples of applications of these ultrasound-based techniques to the field of tissue engineering.

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References

  1. Abraham-Cohn, N., B. Kim, R. Q. Erkamp, D. J. Mooney, S. Y. Emelianov, A. R. Skovoroda, and M. O’Donnell. High-resolution elasticity imaging for tissue engineering. IEEE Trans. Ultrason. Ferr. 47:956–966, 2000.

    Article  CAS  Google Scholar 

  2. Appel, A. A., M. A. Anastasio, J. C. Larson, and E. M. Brey. Imaging challenges in biomaterials and tissue engineering. Biomaterials 34:6615–6630, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Atala, A. Engineering organs. Curr. Opin. Biotechnol. 20:575–592, 2009.

    Article  CAS  PubMed  Google Scholar 

  4. Berco, J., M. Tanter, and M. Fink. Supersonic shear imaging: a new technique for soft tissue elasticity mapping. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 51:1449–1464, 2004.

    Article  Google Scholar 

  5. Brand, S., E. C. Weiss, R. M. Lemor, and M. C. Kolios. High frequency ultrasound tissue characterization and acoustic microscopy of intracellular changes. Ultrasound Med. Biol. 34:1396–1407, 2008.

    Article  PubMed  Google Scholar 

  6. Chen, S., M. Fatemi, and J. F. Greenleaf. Shear property characterization of viscoelastic media using vibrations induced by ultrasound radiation force. Proceedings of the IEEE International Ultrasonics Symposium, pp. 1871–1875, 2002.

  7. Chung, E., S. Y. Nam, L. M. Ricles, S. Y. Emelianov, and L. J. Suggs. Evaluation of gold nanotracers to track adipose-derived stem cells in a PEGylated fibrin gel for dermal tissue engineering applications. Int. J. Nanomed. 8:325–336, 2013.

    Article  Google Scholar 

  8. Czarnota, G. J., M. C. Kolios, J. Abraham, M. Portnoy, F. P. Ottensmeyer, J. W. Hunt, and M. D. Sherar. Ultrasound imaging of apoptosis: high-resolution non-invasive monitoring of programmed cell death in vitro, in situ and in vivo. Br. J. Cancer 81:520–527, 1999.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Dalecki, D. WFUMB Safety Symposium on Echo-Contrast Agents: bioeffects of ultrasound contrast agents in vivo. Ultrasound Med. Biol. 33:205–213, 2007.

    Article  PubMed  Google Scholar 

  10. Discher, D. E., P. Janmey, and Y. L. Wang. Tissue cells feel and respond to the stiffness of their substrate. Science 310:1139–1143, 2005.

    Article  CAS  PubMed  Google Scholar 

  11. Dutta, D., K. W. Lee, R. A. Allen, Y. Wang, J. C. Brigham, and K. Kim. Non-invasive assessment of elastic modulus of arterial constructs during cell culture using ultrasound elasticity imaging. Ultrasound Med. Biol. 39:2103–2115, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  12. Elegbe, E. C., and S. A. McAleavey. Single tracking location methods suppress speckle noise in shear wave velocity estimation. Ultrason. Imaging 35:109–125, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  13. Emelianov, S. Y., P. C. Li, and M. O’Donnell. Photoacoustics for molecular imaging and therapy. Phys. Today 62:34–39, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Fatakdawala, H., L. G. Griffiths, S. Humphrey, and L. Marcu. Time-resolved fluorescence spectroscopy and ultrasound backscatter microscopy for nondestructive evaluation of vascular grafts. J. Biomed. Opt. 19:080503, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  15. Fatemi, M., and J. F. Greenleaf. Probing the dynamics of tissue at low frequencies with the radiation force of ultrasound. Phys. Med. Biol. 45:1449–1464, 2000.

    Article  CAS  PubMed  Google Scholar 

  16. Ferrara, K., R. Pollard, and M. Borden. Ultrasound microbubble contrast agents: fundamentals and application to gene and drug delivery. Annu. Rev. Biomed. Eng. 9:415–447, 2007.

    Article  CAS  PubMed  Google Scholar 

  17. Fite, B. Z., M. Decaris, Y. Sun, A. Lam, C. K. Ho, J. K. Leach, and L. Marcu. Noninvasive multimodal evaluation of bioengineered cartilage constructs combining time-resolved fluorescence and ultrasound imaging. Tissue Eng. Part C Methods. 17:495–504, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Foster, F. S., C. J. Pavlin, K. A. Harasiewicz, D. A. Christopher, and D. H. Turnbull. Advances in ultrasound biomicroscopy. Ultrasound Med. Biol. 26:1–27, 2000.

    Article  CAS  PubMed  Google Scholar 

  19. Gessner, R., and P. A. Dayton. Advances in molecular imaging with ultrasound. Mol. Imaging 9:117–127, 2010.

    PubMed  PubMed Central  Google Scholar 

  20. Gessner, R. C., A. D. Hanson, S. Feingold, A. T. Cashion, A. Corcimaru, B. T. Wu, C. R. Mullins, S. R. Aylward, L. M. Reid, and P. A. Dayton. Functional ultrasound imaging for assessment of extracellular matrix scaffolds used for liver organoid formation. Biomaterials 34:9341–9351, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Ghoshal, G., J. P. Kemmerer, C. Karunakaran, R. Abuhabsah, R. J. Miller, S. Sarwate, and M. L. Oelze. Quantitative ultrasound imaging for monitoring in situ high-intensity focused ultrasound exposure. Ultrason. Imaging 36:239–255, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Ginat, D. T., S. V. Destounis, R. G. Barr, B. Castaneda, J. G. Strang, and D. J. Rubens. US elastography of breast and prostate lesions. Radiographics 29:2007–2016, 2009.

    Article  PubMed  Google Scholar 

  23. Gudur, M., R. R. Rao, Y. S. Hsiao, A. W. Peterson, C. X. Deng, and J. P. Stegemann. Noninvasive, quantitative, spatiotemporal characterization of mineralization in three-dimensional collagen hydrogels using high-resolution spectral ultrasound imaging. Tissue Eng. Part C Methods 18:935–946, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Gudur, M. S., R. R. Rao, A. W. Peterson, D. J. Caldwell, J. P. Stegemann, and C. X. Deng. Noninvasive quantification of in vitro osteoblastic differentiation in 3D engineered tissue constructs using spectral ultrasound imaging. PLoS One 9:e85749, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  25. Guittet, C., O. F. Ossant, L. Vaillant, and M. Berson. In vivo high-frequency ultrasonic characterization of human dermis. IEEE Trans. Biomed. Eng. 46:740–746, 1999.

    Article  CAS  PubMed  Google Scholar 

  26. Hattori, K., Y. Takakura, H. Ohgushi, T. Habata, K. Uematsu, and K. Ikeuchi. Novel ultrasonic evaluation of tissue-engineered cartilage for large osteochondral defects–non-invasive judgment of tissue-engineered cartilage. J. Orthop. Res. 23:1179–1183, 2005.

    Article  PubMed  Google Scholar 

  27. Hoffmann, K., J. Jung, S. el Gammal, and P. Altmeyer. Malignant melanoma in 20-MHz B scan sonography. Dermatology 185:49–55, 1992.

    Article  CAS  PubMed  Google Scholar 

  28. Inkinen, S., J. Liukkonen, J. H. Ylarinne, P. H. Puhakka, M. J. Lammi, T. Viren, J. S. Jurvelin, and J. Toyras. Collagen and chondrocyte concentrations control ultrasound scattering in agarose scaffolds. Ultrasound Med. Biol. 40:2162–2171, 2014.

    Article  CAS  PubMed  Google Scholar 

  29. Insana, M. F., and T. J. Hall. Characterising the microstructure of random media using ultrasound. Phys. Med. Biol. 35:1373–1386, 1990.

    Article  CAS  PubMed  Google Scholar 

  30. Insana, M. F., and T. J. Hall. A method for characterizing soft tissue microstructure using parametric ultrasound imaging. Prog. Clin. Biol. Res. 363:241–256, 1991.

    CAS  PubMed  Google Scholar 

  31. Insana, M. F., R. F. Wagner, D. G. Brown, and T. J. Hall. Describing small-scale structure in random media using pulse-echo ultrasound. J. Acoust. Soc. Am. 87:179–192, 1990.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Kariem, H., M. I. Pastrama, S. I. Roohani-Esfahani, P. Pivonka, H. Zreiqat, and C. Hellmich. Micro-poro-elasticity of baghdadite-based bone tissue engineering scaffolds: a unifying approach based on ultrasonics, nanoindentation, and homogenization theory. Mater. Sci. Eng. C Mater. Biol. Appl. 46:553–564, 2015.

    Article  CAS  PubMed  Google Scholar 

  33. Katouzian, A., S. Sathyanarayana, B. Baseri, E. E. Konofagou, and S. G. Carlier. Challenges in atherosclerotic plaque characterization with intravascular ultrasound (IVUS): from data collection to classification. IEEE Trans. Inf Technol. Biomed. 12:315–327, 2008.

    Article  PubMed  Google Scholar 

  34. Kemmerer, J. P., and M. L. Oelze. Ultrasonic assessment of thermal therapy in rat liver. Ultrasound Med. Biol. 38:2130–2137, 2012.

    Article  PubMed  PubMed Central  Google Scholar 

  35. Kim, K., C. G. Jeong, and S. J. Hollister. Non-invasive monitoring of tissue scaffold degradation using ultrasound elasticity imaging. Acta Biomater. 4:783–790, 2008.

    Article  PubMed  PubMed Central  Google Scholar 

  36. Kolios, M. C., G. J. Czarnota, M. Lee, J. W. Hunt, and M. D. Sherar. Ultrasonic spectral parameter characterization of apoptosis. Ultrasound Med. Biol. 28:589–597, 2002.

    Article  CAS  PubMed  Google Scholar 

  37. Kreitz, S., G. Dohmen, S. Hasken, T. Schmitz-Rode, P. Mela, and S. Jockenhoevel. Nondestructive method to evaluate the collagen content of fibrin-based tissue engineered structures via ultrasound. Tissue Eng. Part C Methods 17:1021–1026, 2011.

    Article  CAS  PubMed  Google Scholar 

  38. Lebertre, M., F. Ossant, L. Vaillant, S. Diridollou, and F. Patat. Spatial variation of acoustic parameters in human skin: an in vitro study between 22 and 45 MHz. Ultrasound Med. Biol. 28:599–615, 2002.

    Article  PubMed  Google Scholar 

  39. Leithem, S. M., R. J. Lavarello, W. D. O’Brien, Jr, and M. L. Oelze. Estimating concentration of ultrasound contrast agents with backscatter coefficients: experimental and theoretical aspects. J. Acoust. Soc. Am. 131:2295–2305, 2012.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Lerner, R. M., S. R. Huang, and K. J. Parker. “Sonoelasticity” images derived from ultrasound signals in mechanically vibrated tissues. Ultrasound Med. Biol. 16:231–239, 1990.

    Article  CAS  PubMed  Google Scholar 

  41. Li, W., M. I. Pastrama, Y. Ding, K. Zheng, C. Hellmich, and A. R. Boccaccini. Ultrasonic elasticity determination of 45S5 Bioglass((R))-based scaffolds: influence of polymer coating and crosslinking treatment. J. Mech. Behav. Biomed. Mater. 40:85–94, 2014.

    Article  PubMed  Google Scholar 

  42. Libgot-Calle, R., F. Ossant, Y. Gruel, P. Lermusiaux, and F. Patat. High frequency ultrasound device to investigate the acoustic properties of whole blood during coagulation. Ultrasound Med. Biol. 34:252–264, 2008.

    Article  PubMed  Google Scholar 

  43. Liu, D., and E. S. Ebbini. Viscoelastic property measurement in thin tissue constructs using ultrasound. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 55:368–383, 2008.

    Article  PubMed  PubMed Central  Google Scholar 

  44. Lizzi, F. L., M. Astor, E. J. Feleppa, M. Shao, and A. Kalisz. Statistical framework for ultrasonic spectral parameter imaging. Ultrasound Med. Biol. 23:1371–1382, 1997.

    Article  CAS  PubMed  Google Scholar 

  45. Lizzi, F. L., M. Astor, T. Liu, C. Deng, D. J. Coleman, and R. H. Silverman. Ultrasonic spectrum analysis for tissue assays and therapy evaluation. Int. J. Imaging Syst. Technol. 8:3–10, 1997.

    Article  Google Scholar 

  46. Lizzi, F. L., M. Greenebaum, E. J. Feleppa, M. Elbaum, and D. J. Coleman. Theoretical framework for spectrum analysis in ultrasonic tissue characterization. J. Acoust. Soc. Am. 73:1366–1373, 1983.

    Article  CAS  PubMed  Google Scholar 

  47. Lizzi, F., M. Ostromogilsky, E. Feleppa, M. Rorke, and M. Yaremko. Relationship of ultrasonic spectral parameters to features of tissue microstructure. IEEE Trans. Ultrason. Ferr. 33:319–329, 1986.

    Google Scholar 

  48. Mallidi, S., S. Kim, A. Karpiouk, P. P. Joshi, K. Sokolov, and S. Emelianov. Visualization of molecular composition and functionality of cancer cells using nanoparticle-augmented ultrasound-guided photoacoustics. Photoacoustics 3:26–34, 2015.

    Article  PubMed  PubMed Central  Google Scholar 

  49. Mamou, J., A. Coron, M. L. Oelze, E. Saegusa-Beecroft, M. Hata, P. Lee, J. Machi, E. Yanagihara, P. Laugier, and E. J. Feleppa. Three-dimensional high-frequency backscatter and envelope quantification of cancerous human lymph nodes. Ultrasound Med. Biol. 37:345–357, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Mathieu, V., F. Anagnostou, E. Soffer, and G. Haiat. Ultrasonic evaluation of dental implant biomechanical stability: an in vitro study. Ultrasound Med. Biol. 37:262–270, 2011.

    Article  PubMed  Google Scholar 

  51. McAleavey, S., E. Collins, J. Kelly, E. Elegbe, and M. Menon. Validation of SMURF estimation of shear modulus in hydrogels. Ultrason. Imaging 31:131–150, 2009.

    Article  PubMed  PubMed Central  Google Scholar 

  52. McAleavey, S. A., M. Menon, and J. Orszulak. Shear-modulus estimation by application of spatially-modulated impulsive acoustic radiation force. Ultrason. Imaging 29:87–104, 2007.

    Article  PubMed  Google Scholar 

  53. Mercado, K. P., M. Helguera, D. C. Hocking, and D. Dalecki. Estimating cell concentration in three-dimensional engineered tissues using high frequency quantitative ultrasound. Ann. Biomed. Eng. 42:1292–1304, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Mercado, K. P., M. Helguera, D. C. Hocking, and D. Dalecki. Noninvasive quantitative imaging of collagen microstructure in three-dimensional hydrogels using high-frequency ultrasound. Tissue Eng. Part C Methods 21(7):671–682, 2015.

    Article  CAS  PubMed  Google Scholar 

  55. Mercado, K. P., J. Langdon, M. Helguera, S. A. McAleavey, D. C. Hocking, and D. Dalecki. Scholte wave generation during single tracking location shear wave elasticity imaging of engineered tissues. JASA Express Lett. 138:EL138, 2015.

    Google Scholar 

  56. Miron-Mendoza, M., J. Seemann, and F. Grinnell. The differential regulation of cell motile activity through matrix stiffness and porosity in three dimensional collagen matrices. Biomaterials 31:6425–6435, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Nam, S. Y., E. Chung, L. J. Suggs, and S. Y. Emelianov. Combined ultrasound and photoacoustic imaging to noninvasively assess burn injury and selectively monitor a regenerative tissue-engineered construct. Tissue Eng. Part C Methods. 21:557–566, 2015.

    Article  CAS  PubMed  Google Scholar 

  58. Nam, S. Y., L. M. Ricles, L. J. Suggs, and S. Y. Emelianov. Imaging strategies for tissue engineering applications. Tissue Eng. Part B Rev. 21:88–102, 2015.

    Article  PubMed  PubMed Central  Google Scholar 

  59. Nightingale, K. R., M. L. Palmeri, R. W. Nightingale, and G. E. Trahey. On the feasibility of remote palpation using acoustic radiation force. J. Acoust. Soc. Am. 110:625–634, 2001.

    Article  CAS  PubMed  Google Scholar 

  60. Nyborg, W. WFUMB Safety Symposium on Echo-Contrast Agents: mechanisms for the interaction of ultrasound. Ultrasound Med. Biol. 33:224–232, 2007.

    Article  PubMed  Google Scholar 

  61. Oe, K., M. Miwa, K. Nagamune, Y. Sakai, S. Y. Lee, T. Niikura, T. Iwakura, T. Hasegawa, N. Shibanuma, Y. Hata, R. Kuroda, and M. Kurosaka. Nondestructive evaluation of cell numbers in bone marrow stromal cell/beta-tricalcium phosphate composites using ultrasound. Tissue Eng. Part C Methods. 16:347–353, 2010.

    Article  CAS  PubMed  Google Scholar 

  62. Palmeri, M. L., S. A. McAleavey, G. E. Trahey, and K. R. Nightingale. Ultrasonic tracking of acoustic radiation force-induced displacements in homogeneous media. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 53:1300–1313, 2006.

    Article  PubMed  PubMed Central  Google Scholar 

  63. Park, D. W., S. H. Ye, H. B. Jiang, D. Dutta, K. Nonaka, W. R. Wagner, and K. Kim. In vivo monitoring of structural and mechanical changes of tissue scaffolds by multi-modality imaging. Biomaterials 35:7851–7859, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Parker, K. J., M. M. Doyley, and D. J. Rubens. Imaging the elastic properties of tissue: the 20 year perspective. Phys. Med. Biol. 56:R1–R29, 2011.

    Article  CAS  PubMed  Google Scholar 

  65. Pavlin, C. J., K. Harasiewicz, M. D. Sherar, and F. S. Foster. Clinical use of ultrasound biomicroscopy. Ophthalmology 98:287–295, 1991.

    Article  CAS  PubMed  Google Scholar 

  66. Potkin, B. N., A. L. Bartorelli, J. M. Gessert, R. F. Neville, Y. Almagor, W. C. Roberts, and M. B. Leon. Coronary artery imaging with intravascular high-frequency ultrasound. Circulation 81:1575–1585, 1990.

    Article  CAS  PubMed  Google Scholar 

  67. Qin, S., C. F. Caskey, and K. W. Ferrara. Ultrasound contrast microbubbles in imaging and therapy: physical principles and engineering. Phys. Med. Biol. 54:R27–R57, 2009.

    Article  PubMed  PubMed Central  Google Scholar 

  68. Rice, M. A., K. R. Waters, and K. S. Anseth. Ultrasound monitoring of cartilaginous matrix evolution in degradable PEG hydrogels. Acta Biomater. 5:152–161, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Rooney, J. A., and W. L. Nyborg. Acoustic radiation pressure in a travelling plane-wave. Am. J. Phys. 40:1825–1830, 1972.

    Article  Google Scholar 

  70. Sarvazyan, A. P., O. V. Rudenko, S. D. Swanson, J. B. Fowlkes, and S. Y. Emelianov. Shear wave elasticity imaging: a new ultrasonic technology of medical diagnostics. Ultrasound Med. Biol. 24:1419–1435, 1998.

    Article  CAS  PubMed  Google Scholar 

  71. Sherar, M. D., B. G. Starkoski, W. B. Taylor, and F. S. Foster. A 100 MHz B-scan ultrasound backscatter microscope. Ultrason. Imaging 11:95–105, 1989.

    Article  CAS  PubMed  Google Scholar 

  72. Solorio, L., B. M. Babin, R. B. Patel, J. Mach, N. Azar, and A. A. Exner. Noninvasive characterization of in situ forming implants using diagnostic ultrasound. J. Control Release 143:183–190, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Sun, Y., D. Responte, H. Xie, J. Liu, H. Fatakdawala, J. Hu, K. A. Athanasiou, and L. Marcu. Nondestructive evaluation of tissue engineered articular cartilage using time-resolved fluorescence spectroscopy and ultrasound backscatter microscopy. Tissue Eng. Part C Methods. 18:215–226, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Taggart, L. R., R. E. Baddour, A. Giles, G. J. Czarnota, and M. C. Kolios. Ultrasonic characterization of whole cells and isolated nuclei. Ultrasound Med. Biol. 33:389–401, 2007.

    Article  PubMed  Google Scholar 

  75. Talukdar, Y., P. Avti, J. Sun, and B. Sitharaman. Multimodal ultrasound-photoacoustic imaging of tissue engineering scaffolds and blood oxygen saturation in and around the scaffolds. Tissue Eng. Part C Methods. 20:440–449, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Tanaka, Y., Y. Saijo, Y. Fujihara, H. Yamaoka, S. Nishizawa, S. Nagata, T. Ogasawara, Y. Asawa, T. Takato, and K. Hoshi. Evaluation of the implant type tissue-engineered cartilage by scanning acoustic microscopy. J. Biosci. Bioeng. 113:252–257, 2012.

    Article  CAS  PubMed  Google Scholar 

  77. Tunis, A. S., G. J. Czarnota, A. Giles, M. D. Sherar, J. W. Hunt, and M. C. Kolios. Monitoring structural changes in cells with high-frequency ultrasound signal statistics. Ultrasound Med. Biol. 31:1041–1049, 2005.

    Article  CAS  PubMed  Google Scholar 

  78. Vayron, R., E. Soffer, F. Anagnostou, and G. Haiat. Ultrasonic evaluation of dental implant osseointegration. J. Biomech. 47:3562–3568, 2014.

    Article  PubMed  Google Scholar 

  79. Vlad, R. M., S. Brand, A. Giles, M. C. Kolios, and G. J. Czarnota. Quantitative ultrasound characterization of responses to radiotherapy in cancer mouse models. Clin. Cancer Res. 15:2067–2075, 2009.

    Article  CAS  PubMed  Google Scholar 

  80. Vlad, R. M., M. C. Kolios, J. L. Moseley, G. J. Czarnota, and K. K. Brock. Evaluating the extent of cell death in 3D high frequency ultrasound by registration with whole-mount tumor histopathology. Med. Phys. 37:4288–4297, 2010.

    Article  PubMed  Google Scholar 

  81. Walker, J. M., A. M. Myers, M. D. Schluchter, V. M. Goldberg, A. I. Caplan, J. A. Berilla, J. M. Mansour, and J. F. Welter. Nondestructive evaluation of hydrogel mechanical properties using ultrasound. Ann. Biomed. Eng. 39:2521–2530, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  82. Wang, J. H., C. S. Changchien, C. H. Hung, H. L. Eng, W. C. Tung, K. M. Kee, C. H. Chen, T. H. Hu, C. M. Lee, and S. N. Lu. FibroScan and ultrasonography in the prediction of hepatic fibrosis in patients with chronic viral hepatitis. J. Gastroenterol. 44:439–446, 2009.

    Article  PubMed  Google Scholar 

  83. Wilson, K., K. Homan, and S. Emelianov. Biomedical photoacoustics beyond thermal expansion using triggered nanodroplet vaporization for contrast-enhanced imaging. Nat Commun. 3:618, 2012.

    Article  PubMed  Google Scholar 

  84. Winterroth, F., K. W. Hollman, S. Kuo, K. Izumi, S. E. Feinberg, S. J. Hollister, and J. B. Fowlkes. Comparison of scanning acoustic microscopy and histology images in characterizing surface irregularities among engineered human oral mucosal tissues. Ultrasound Med. Biol. 37:1734–1742, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  85. Winterroth, F., J. Lee, S. Kuo, J. B. Fowlkes, S. E. Feinberg, S. J. Hollister, and K. W. Hollman. Acoustic microscopy analyses to determine good vs. failed tissue engineered oral mucosa under normal or thermally stressed culture conditions. Ann. Biomed. Eng. 39:44–52, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  86. Wu, Z., L. S. Taylor, D. J. Rubens, and K. J. Parker. Sonoelastographic imaging of interference patterns for estimation of the shear velocity of homogeneous biomaterials. Phys. Med. Biol. 49:911–922, 2004.

    Article  PubMed  Google Scholar 

  87. Yu, J., K. Takanari, Y. Hong, K. W. Lee, N. J. Amoroso, Y. Wang, W. R. Wagner, and K. Kim. Non-invasive characterization of polyurethane-based tissue constructs in a rat abdominal repair model using high frequency ultrasound elasticity imaging. Biomaterials 34:2701–2709, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Zhang, D., X. Gong, and S. Ye. Acoustic nonlinearity parameter tomography for biological specimens via measurements of the second harmonics. J. Acoust. Soc. Am. 99:2397–2402, 1996.

    Article  CAS  PubMed  Google Scholar 

  89. Zhou, H., M. Goss, C. Hernandez, J.M. Mansour and A. Exner. Validation of ultrasound elastography imaging for nondestructive characterization of stiffer biomaterials. Ann Biomed Eng., 2015.

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Acknowledgments

This work was supported, in part, by a grant from the National Institutes of Health (R01 EB018210).

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Correspondence to Diane Dalecki.

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Associate Editor Agata Exner oversaw the review of this article.

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Dalecki, D., Mercado, K.P. & Hocking, D.C. Quantitative Ultrasound for Nondestructive Characterization of Engineered Tissues and Biomaterials. Ann Biomed Eng 44, 636–648 (2016). https://doi.org/10.1007/s10439-015-1515-0

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