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Application of Elastography for the Noninvasive Assessment of Biomechanics in Engineered Biomaterials and Tissues

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

The elastic properties of engineered biomaterials and tissues impact their post-implantation repair potential and structural integrity, and are critical to help regulate cell fate and gene expression. The measurement of properties (e.g., stiffness or shear modulus) can be attained using elastography, which exploits noninvasive imaging modalities to provide functional information of a material indicative of the regeneration state. In this review, we outline the current leading elastography methodologies available to characterize the properties of biomaterials and tissues suitable for repair and mechanobiology research. We describe methods utilizing magnetic resonance, ultrasound, and optical coherent elastography, highlighting their potential for longitudinal monitoring of implanted materials in vivo, in addition to spatiotemporal limits of each method for probing changes in cell-laden constructs. Micro-elastography methods now allow acquisitions at length scales approaching 5–100 μm in two and three dimensions. Many of the methods introduced in this review are therefore capable of longitudinal monitoring in biomaterials and tissues approaching the cellular scale. However, critical factors such as anisotropy, heterogeneity and viscoelasity—inherent in many soft tissues—are often not fully described and therefore require further advancements and future developments.

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References

  1. Abraham Cohn, N., B. S. 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. Ferroelectr. Freq. Control 47:956–966, 2000.

    Article  CAS  PubMed  Google Scholar 

  2. Adamczyk, M. M., T. C. Lee, and I. Vesely. Biaxial strain properties of elastase-digested porcine aortic valves. J. Heart Valve Dis. 9:445–453, 2000.

    CAS  PubMed  Google Scholar 

  3. Adie, S. G., B. F. Kennedy, J. J. Armstrong, S. A. Alexandrov, and D. D. Sampson. Audio frequency in vivo optical coherence elastography. Phys. Med. Biol. 54:3129–3139, 2009.

    Article  PubMed  Google Scholar 

  4. Adie, S. G., X. Liang, B. F. Kennedy, R. John, D. D. Sampson, and S. A. Boppart. Spectroscopic optical coherence elastography. Opt. Express 18:25519–25534, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Aglyamov, S. R., R. Bouchard, I. Graf, and S. Y. Emelianov. Breast elasticity imaging. In: Physics of Mammographic Imaging, edited by M. K. Markey. Boca Raton: CRC Press, 2012, p. 223.

    Google Scholar 

  6. Ahmad, A., J. Kim, N. A. Sobh, N. D. Shemonski, and S. A. Boppart. Magnetomotive optical coherence elastography using magnetic particles to induce mechanical waves. Biomed. Opt. Express 5:2349, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  7. Aletras, A. H., S. Ding, R. S. Balaban, and H. Wen. DENSE: displacement encoding with stimulated echoes in cardiac functional MRI. J. Magn. Reson. 137:247–252, 1999.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Alonso-Caneiro, D., K. Karnowski, B. J. Kaluzny, A. Kowalczyk, and M. Wojtkowski. Assessment of corneal dynamics with high-speed swept source Optical Coherence Tomography combined with an air puff system. Opt. Express 19:14188, 2011.

    Article  CAS  PubMed  Google Scholar 

  9. Axel, L. Biomechanical dynamics of the heart with MRI. Annu. Rev. Biomed. Eng. 4:321–347, 2002.

    Article  CAS  PubMed  Google Scholar 

  10. Axel, L., and L. Dougherty. MR imaging of motion with spatial modulation of magnetization. Radiology 171:841–845, 1989.

    Article  CAS  PubMed  Google Scholar 

  11. Bercoff, J., M. Tanter, and M. Fink. Supersonic shear imaging: a new technique for soft tissue elasticity mapping. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 51:396–409, 2004.

    Article  PubMed  Google Scholar 

  12. Berg, E. P., F. Kallel, F. Hussain, R. K. Miller, J. Ophir, and N. Kehtarnavaz. The use of elastography to measure quality characteristics of pork semimembranosus muscle. Meat Sci. 53:31–35, 1999.

    Article  CAS  PubMed  Google Scholar 

  13. Bilgen, M., and M. F. Insana. Error analysis in acoustic elastography. II. Strain estimation and SNR analysis. J. Acoust. Soc. Am. 101:1147–1154, 1997.

    Article  CAS  PubMed  Google Scholar 

  14. Bilgen, M., S. Srinivasan, L. B. Lachman, and J. Ophir. Elastography imaging of small animal oncology models: a feasibility study. Ultrasound Med. Biol. 29:1291–1296, 2003.

    Article  PubMed  Google Scholar 

  15. Briggs, B. N., M. E. Stender, P. M. Muljadi, M. A. Donnelly, V. D. Winn, and V. L. Ferguson. A Hertzian contact mechanics based formulation to improve ultrasound elastography assessment of uterine cervical tissue stiffness. J. Biomech. 48:1524–1532, 2015.

    Article  PubMed  Google Scholar 

  16. Butz, K. D., D. D. Chan, E. A. Nauman, and C. P. Neu. Stress distributions and material properties determined in articular cartilage from MRI-based finite strains. J. Biomech. 44(15):2667–2672, 2011.

    Article  PubMed  Google Scholar 

  17. Cai L., C. Pedersen, R. Mclendon, M. Biedermann, G. Dimitrova, J. Yao and C. P. Neu. Stiffness characterization in biological materials based on deformation imaging and topology optimization. In: Summer Biomechanics, Bioengineering and Biotransport Conference. Snowbird Resort, Utah, USA, 2015.

  18. Calve S., A. Ready, C. Huppenbauer, R. Main and C. P. Neu. Optical clearing in dense connective tissues to visualize cellular connectivity in situ. Plos One. 10(1):e0116662, 2015. doi:10.1371/journal.pone.0116662.

    Article  CAS  Google Scholar 

  19. Canovic, E. P., D. T. Seidl, S. R. Polio, A. A. Oberai, P. E. Barbone, D. Stamenovic, and M. L. Smith. Biomechanical imaging of cell stiffness and prestress with subcellular resolution. Biomech. Model. Mechanobiol. 13:665–678, 2014.

    Article  PubMed  Google Scholar 

  20. Casula G. and J. M. Carcione. Generalized mechanical model analogies of linear viscoelastic behaviour. Bollettino di geofisica teorica ed applicata 1992.

  21. Cespedes, I., J. Ophir, H. Ponnekanti, and N. Maklad. Elastography: elasticity imaging using ultrasound with application to muscle and breast in vivo. Ultrason. Imaging 15:73–88, 1993.

    Article  CAS  PubMed  Google Scholar 

  22. Chan D. D., K. D. Butz, S. Trippel, E. A. Nauman and C. P. Neu. In vivo displacements and strains measured in human knee articular cartilage using dualMRI. In: Annual Meeting of the Orthopaedic Research Society. New Orleans, LA, 2014.

  23. Chan, D. D., L. Cai, K. D. Butz, S. B. Trippel, E. A. Nauman, and C. P. Neu. In vivo articular cartilage deformation: noninvasive quantification of intratissue strain during joint contact in the human knee. Sci. Rep. 6:19220, 2016. doi:10.1038/srep19220.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Chan, D. D., S. N. Khan, X. Ye, S. B. Curtiss, M. C. Gupta, E. O. Klineberg, and C. P. Neu. Mechanical deformation and glycosaminoglycan content changes in a rabbit annular puncture disc degeneration model. Spine 36:1438–1445, 2011.

    Article  PubMed  Google Scholar 

  25. Chan, Q. C. C., G. Li, R. L. Ehman, R. C. Grimm, R. Li, and E. S. Yang. Needle shear wave driver for magnetic resonance elastography. Magn. Reson. Med. 55:1175–1179, 2006.

    Article  CAS  PubMed  Google Scholar 

  26. Chan Q. C. C., G. Li, R. L. Ehman, P. J. Rossman, G. Cao, R. Li, E. S. Yang and IEEE. Shear waves induced by moving needle in MR Elastography. In: Proceedings of the 26th Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Vols 1-7, 2004, pp. 1022–1024.

  27. Chan, D. D., and C. P. Neu. Transient and microscale deformations and strains measured under exogenous loading by noninvasive magnetic resonance. PLoS One 7:e33463, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Chan, D. D., C. P. Neu, and M. L. Hull. Articular cartilage deformation determined in an intact tibiofemoral joint by displacement-encoded imaging. Magn. Reson. Med. 61:989–993, 2009.

    Article  PubMed  PubMed Central  Google Scholar 

  29. Chan, D. D., C. P. Neu, and M. L. Hull. In situ deformation of cartilage in cyclically loaded tibiofemoral joints by displacement-encoded MRI. Osteoarthr. Cartil. 17:1461–1468, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Chaturvedi, P., M. F. Insana, and T. J. Hall. 2D companding for noise reduction in strain imaging. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 45:179–191, 1998.

    Article  CAS  PubMed  Google Scholar 

  31. Chen, X., Y. Shen, Y. Zheng, H. Lin, Y. Guo, Y. Zhu, X. Zhang, T. Wang, and S. Chen. Quantification of liver viscoelasticity with acoustic radiation force: a study of hepatic fibrosis in a rat model. Ultrasound Med. Biol. 39:2091–2102, 2013.

    Article  PubMed  Google Scholar 

  32. Chernak, S. L., and D. G. Thelen. The use of 2D ultrasound elastography for measuring tendon motion and strain. J. Biomech. 47:750–754, 2014.

    Article  Google Scholar 

  33. Chhetri, R. K., J. Carpenter, R. Superfine, S. H. Randell, and A. L. Oldenburg. Magnetomotive optical coherence elastography for relating lung structure and function in Cystic Fibrosis. Proc. SPIE Int. Soc. Opt. Eng. 7554:755420, 2010.

    PubMed  PubMed Central  Google Scholar 

  34. Chino, K., R. Akagi, M. Dohi, S. Fukashiro, and H. Takahashi. Reliability and validity of quantifying absolute muscle hardness using ultrasound elastography. PLoS One 7:e45764, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Cochlin, D. L., R. Ganatra, and D. Griffiths. Elastography in the detection of prostatic cancer. Clin. Radiol. 57:1014–1020, 2002.

    Article  PubMed  Google Scholar 

  36. Cogollo, J. F. S., M. Tedesco, S. Martinoia, and R. Raiteri. A new integrated system combining atomic force microscopy and micro-electrode array for measuring the mechanical properties of living cardiac myocytes. Biomed. Microdev. 13:613–621, 2011.

    Article  Google Scholar 

  37. Cox, T. R., and J. T. Erler. Remodeling and homeostasis of the extracellular matrix: implications for fibrotic diseases and cancer. Dis. Model. Mech. 4:165–178, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Crecea, V., A. L. Oldenburg, X. Liang, T. S. Ralston, and S. A. Boppart. Magnetomotive nanoparticle transducers for optical rheology of viscoelastic materials. Opt. Express 17:23114–23122, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Curtis, E. T., S. Zhang, V. Khalilzad-Sharghi, T. Boulet, and S. F. Othman. Magnetic resonance elastography methodology for the evaluation of tissue engineered construct growth. J. Vis. Exp. 3:23–216, 2012.

    Google Scholar 

  40. Doherty, J. R., G. E. Trahey, K. R. Nightingale, and M. L. Palmeri. Acoustic radiation force elasticity imaging in diagnostic ultrasound. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 60:685–701, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Dorronsoro, C., D. Pascual, P. Perez-Merino, S. Kling, and S. Marcos. Dynamic OCT measurement of corneal deformation by an air puff in normal and cross-linked corneas. Biomed. Opt. Express 3:473–487, 2012.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Doyley, M. M. Model-based elastography: a survey of approaches to the inverse elasticity problem. Phys. Med. Biol. 57:R35–R73, 2012.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Drakonaki, E. E., G. M. Allen, and D. J. Wilson. Real-time ultrasound elastography of the normal Achilles tendon: reproducibility and pattern description. Clin. Radiol. 64:1196–1202, 2009.

    Article  CAS  PubMed  Google Scholar 

  44. 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 

  45. Egeblad, M., M. G. Rasch, and V. M. Weaver. Dynamic interplay between the collagen scaffold and tumor evolution. Curr. Opin. Cell Biol. 22:697–706, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Engler, A. J., S. Sen, H. L. Sweeney, and D. E. Discher. Matrix elasticity directs stem cell lineage specification. Cell 126:677–689, 2006.

    Article  CAS  PubMed  Google Scholar 

  47. Fercher, A. F., W. Drexler, C. K. Hitzenberger, and T. Lasser. Optical coherence tomography-principles and applications. Rep. Prog. Phys. 66:239, 2003.

    Article  Google Scholar 

  48. Fink, M., and M. Tanter. Multiwave imaging and super resolution. Phys. Today 63:28–33, 2010.

    Article  Google Scholar 

  49. Fujimoto, J. G., C. Pitris, S. A. Boppart, and M. E. Brezinski. Optical coherence tomography: an emerging technology for biomedical imaging and optical biopsy. Neoplasia 2:9–25, 2000.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Garra, B. S., E. I. Cespedes, J. Ophir, S. R. Spratt, R. A. Zuurbier, C. M. Magnant, and M. F. Pennanen. Elastography of breast lesions: initial clinical results. Radiology 202:79–86, 1997.

    Article  CAS  PubMed  Google Scholar 

  51. Griebel, A. J., M. Khoshgoftar, T. Novak, C. C. van Donkelaar, and C. P. Neu. Direct noninvasive measurement and numerical modeling of depth-dependent strains in layered agarose constructs. J. Biomech. 47:2149–2156, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Griebel, A. J., S. B. Trippel, N. C. Emery, and C. P. Neu. Noninvasive assessment of osteoarthritis severity in human explants by multicontrast MRI. Magn. Reson. Med. 71:807–814, 2013.

    Article  Google Scholar 

  53. Griebel, A. J., S. B. Trippel, and C. P. Neu. Noninvasive dualMRI-based strains vary by depth and region in human osteoarthritic articular cartilage. Osteoarthr. Cartil. 21:394–400, 2013.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Guan, G., C. Li, Y. Ling, Y. Yang, J. B. Vorstius, R. P. Keatch, R. K. Wang, and Z. Huang. Quantitative evaluation of degenerated tendon model using combined optical coherence elastography and acoustic radiation force method. J. Biomed. Opt. 18:111417, 2013.

    Article  PubMed  Google Scholar 

  55. Guilak, F., D. M. Cohen, B. T. Estes, J. M. Gimble, W. Liedtke, and C. S. Chen. Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem Cell 5:17–26, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Guvendiren, M., M. Perepelyuk, R. G. Wells, and J. A. Burdick. Hydrogels with differential and patterned mechanics to study stiffness-mediated myofibroblastic differentiation of hepatic stellate cells. J. Mech. Behav. Biomed. Mater. 38:198–208, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Hardy, P. A., A. C. Ridler, C. B. Chiarot, D. B. Plewes, and R. M. Henkelman. Imaging articular cartilage under compression—Cartilage elastography. Magn. Reson. Med. 53:1065–1073, 2005.

    Article  PubMed  Google Scholar 

  58. Hee, L., P. Sandager, O. Petersen, and N. Uldbjerg. Quantitative sonoelastography of the uterine cervix by interposition of a synthetic reference material. Acta Obstet. Gynecol. Scand. 92:1244–1249, 2013.

    Article  PubMed  Google Scholar 

  59. Hollman, K. W., R. M. Shtein, S. Tripathy, and K. Kim. Using an ultrasound elasticity microscope to map three-dimensional strain in a porcine cornea. Ultrasound Med. Biol. 39:1451–1459, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  60. Huang, H. Y., B. N. Balhouse, and S. Huang. Application of simple biomechanical and biochemical tests to heart valve leaflets: implications for heart valve characterization and tissue engineering. Proc. Inst. Mech. Eng. H 226:868–876, 2012.

    Article  PubMed  Google Scholar 

  61. Huang, D., E. A. Swanson, C. P. Lin, J. S. Schuman, W. G. Stinson, W. Chang, M. R. Hee, T. Flotte, K. Gregory, and C. A. Puliafito. Optical coherence tomography. Science 254:1178–1181, 1991.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Jha, A. K., R. A. Hule, T. Jiao, S. S. Teller, R. J. Clifton, R. L. Duncan, D. J. Pochan, and X. Jia. Structural analysis and mechanical characterization of hyaluronic acid-based doubly cross-linked networks. Macromolecules 42:537–546, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Jiming Z. and M. Raja. Magnetic resonance elastography. In: Handbook of Imaging in Biological Mechanics, CRC Press, 2014, pp. 33–54.

  64. Karamichos, D., R. Brown, and V. Mudera. Collagen stiffness regulates cellular contraction and matrix remodeling gene expression. J. Biomed. Mater. Res. Part A 83:887–894, 2007.

    Article  CAS  Google Scholar 

  65. Kennedy, B. F., T. R. Hillman, R. A. McLaughlin, B. C. Quirk, and D. D. Sampson. In vivo dynamic optical coherence elastography using a ring actuator. Opt. Express 17:21762–21772, 2009.

    Article  CAS  PubMed  Google Scholar 

  66. Kennedy, B. F., X. Liang, S. G. Adie, D. K. Gerstmann, B. C. Quirk, S. A. Boppart, and D. D. Sampson. In vivo three-dimensional optical coherence elastography. Opt. Express 19:6623–6634, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Kennedy, K. M., R. A. McLaughlin, B. F. Kennedy, A. Tien, B. Latham, C. M. Saunders, and D. D. Sampson. Needle optical coherence elastography for the measurement of microscale mechanical contrast deep within human breast tissues. J. Biomed. Opt. 18:121510–121510, 2013.

    Article  PubMed  Google Scholar 

  68. Kim W., L. Cai, D. McMillan, G. Tamer and C. P. Neu. In vivo measurement of two-dimensional strain in adjacent human intervertebral discs during flexion. In: Annual Meeting of the Orthopaedic Research Society. Las Vegas, 2014.

  69. 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 

  70. Ko H. J., W. Tan, R. Stack and S. A. Boppart. Optical coherence elastography of developing biological tissues. In: Coherence Domain Optical Methods and Optical Coherence Tomography in Biomedicine IX, edited by V. V. Tuchin, J. A. Izatt and J. G. Fujimoto, 2005, pp. 187–194.

  71. Ko, H. J., W. Tan, R. Stack, and S. A. Boppart. Optical coherence elastography of engineered and developing tissue. Tissue Eng. 12:63–73, 2006.

    Article  PubMed  Google Scholar 

  72. Korhonen, R., M. Laasanen, J. Töyräs, J. Rieppo, J. Hirvonen, H. Helminen, and J. Jurvelin. Comparison of the equilibrium response of articular cartilage in unconfined compression, confined compression and indentation. J. Biomech. 35:903–909, 2002.

    Article  CAS  PubMed  Google Scholar 

  73. Lee, B. H., M. H. Kim, J. H. Lee, D. Seliktar, N. J. Cho, and L. P. Tan. Modulation of Huh7.5 spheroid formation and functionality using modified PEG-based hydrogels of different stiffness. PLoS One 10(2):e0118123, 2015.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  74. Lee K.-W. and Y. Wang. Elastomeric PGS scaffolds in arterial tissue engineering. J. Vis. Exp., JoVE. 2691, 2011. doi:10.3791/2691.

  75. Li, C., G. Guan, Z. Huang, M. Johnstone, and R. K. Wang. Noncontact all-optical measurement of corneal elasticity. Opt. Lett. 37:1625–1627, 2012.

    Article  PubMed  Google Scholar 

  76. Li, C., Z. Huang, and R. K. Wang. Elastic properties of soft tissue-mimicking phantoms assessed by combined use of laser ultrasonics and low coherence interferometry. Opt. Express 19:10153–10163, 2011.

    Article  CAS  PubMed  Google Scholar 

  77. Li, J., S. Wang, M. Singh, S. Aglyamov, S. Emelianov, M. Twa, and K. Larin. Air-pulse OCE for assessment of age-related changes in mouse cornea in vivo. Laser Phys. Lett. 11:065601, 2014.

    Article  Google Scholar 

  78. Li J. S., S. Wang, M. Singh, S. Aglyamov, S. Emelianov, M. Twa and K. V. Larin. Air puff OCE for assessment of mouse cornea in vivo. Ophthalmic Technologies Xxiv 8930: 2014.

  79. Liang, X., A. L. Oldenburg, V. Crecea, E. J. Chaney, and S. A. Boppart. Optical micro-scale mapping of dynamic biomechanical tissue properties. Opt. Express 16:11052–11065, 2008.

    Article  PubMed  PubMed Central  Google Scholar 

  80. Lopez, O., K. K. Amrami, A. Manduca, and R. L. Ehman. Characterization of the dynamic shear properties of hyaline cartilage using high-frequency dynamic MR elastography. Magn. Reson. Med. 59:356–364, 2008.

    Article  PubMed  Google Scholar 

  81. Lopez, O., K. K. Amrami, A. Manduca, P. J. Rossman, and R. L. Ehman. Developments in dynamic MR elastography for in vitro biomechanical assessment of hyaline cartilage under high-frequency cyclical shear. J. Magn. Reson. Imaging 25:310–320, 2007.

    Article  PubMed  Google Scholar 

  82. Lopez O., K. Amrami, P. Rossman and R. L. Ehman. Using magnetic resonance elastography to assess the dynamic mechanical properties of cartilage. In: Medical Imaging 2004: Physiology, Function, and Structure from Medical Images, edited by A. A. Amini and A. Manduca, 2004, pp. 51–61.

  83. Lopez O., P. J. Rossman and R. L. Ehman. Dynamic MR elastography of cartilage. In: Proceedings of the 11th Annual Meeting of ISMRM 2003.

  84. Lu, M. H., W. Yu, Q. H. Huang, Y. P. Huang, and Y. P. Zheng. A hand-held indentation system for the assessment of mechanical properties of soft tissues in vivo. IEEE Trans. Instrum. Meas. 58:3079–3085, 2009.

    Article  Google Scholar 

  85. Manapuram, R. K., S. R. Aglyamov, F. M. Monediado, M. Mashiatulla, J. Li, S. Y. Emelianov, and K. V. Larina. In vivo estimation of elastic wave parameters using phase-stabilized swept source optical coherence elastography. J. Biomed. Opt. 17:100501, 2012.

    Article  PubMed  PubMed Central  Google Scholar 

  86. Mariappan, Y. K., K. J. Glaser, A. Manduca, A. J. Romano, S. K. Venkatesh, M. Yin, and R. L. Ehman. High-frequency mode conversion technique for stiff lesion detection with magnetic resonance elastography (MRE). Magn. Reson. Med. 62:1457–1465, 2009.

    Article  PubMed  PubMed Central  Google Scholar 

  87. Mauldin, F. W., M. A. Haider, E. G. Loboa, R. H. Behler, L. E. Euliss, T. W. Pfeiler, and C. M. Gallippi. Monitored steady-state excitation and recovery (MSSER) radiation force imaging using viscoelastic models. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 55:1597–1610, 2008.

    Article  PubMed  Google Scholar 

  88. McCredie A. J., E. Stride, N. Saffari and IEEE. Ultrasound elastography to determine the layered mechanical properties of articular cartilage and the importance of such structural characteristics under load. In: 2009 Annual International Conference of the IEEE Engineering in Medicine and Biology Society, Vol. 1–20, 2009, pp. 4262–4265.

  89. McKnight, A. L., J. L. Kugel, P. J. Rossman, A. Manduca, L. C. Hartmann, and R. L. Ehman. MR elastography of breast cancer: preliminary results. Am. J. Roentgenol. 178:1411–1417, 2002.

    Article  Google Scholar 

  90. Mikula, E., K. Hollman, D. Chai, J. V. Jester, and T. Juhasz. Measurement of corneal elasticity with an acoustic radiation force elasticity microscope. Ultrasound Med. Biol. 40:1671–1679, 2014.

    Article  PubMed  Google Scholar 

  91. Montaldo, G., M. Tanter, J. Bercoff, N. Benech, and M. Fink. Coherent plane-wave compounding for very high frame rate ultrasonography and transient elastography. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 56:489–506, 2009.

    Article  PubMed  Google Scholar 

  92. Muraki, T., H. Ishikawa, S. Morise, N. Yamamoto, H. Sano, E. Itoi, and S. Izumi. Ultrasound elastography-based assessment of the elasticity of the supraspinatus muscle and tendon during muscle contraction. J. Shoulder Elbow Surg. 24:120–126, 2015.

    Article  PubMed  Google Scholar 

  93. Murphy, M. C., J. Huston, C. R. Jack, K. J. Glaser, A. Manduca, J. P. Felmlee, and R. L. Ehman. Decreased brain stiffness in Alzheimer’s disease determined by magnetic resonance elastography. J. Magn. Reson. Imaging 34:494–498, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  94. Muthupillai, R., D. J. Lomas, P. J. Rossman, J. F. Greenleaf, A. Manduca, and R. L. Ehman. Magnetic resonance elastography by direct visualization of propagating acoustic strain waves. Science 269:1854–1857, 1995.

    Article  CAS  PubMed  Google Scholar 

  95. Muthupillai, R., P. J. Rossman, D. J. Lomas, J. F. Greenleaf, S. J. Riederer, and R. L. Ehman. Magnetic resonance imaging of transverse acoustic strain waves. Magn. Reson. Med. 36:266–274, 1996.

    Article  CAS  PubMed  Google Scholar 

  96. Neu, C. P., H. F. Arastu, S. Curtiss, and A. H. Reddi. Characterization of engineered tissue construct mechanical function by magnetic resonance imaging. J. Tissue Eng. Regen. Med. 3:477–485, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Neu, C. P., and M. L. Hull. Toward an MRI-based method to measure non-uniform cartilage deformation: an MRI-cyclic loading apparatus system and steady-state cyclic displacement of articular cartilage under compressive loading. J. Biomech. Eng. 125:180–188, 2003.

    Article  CAS  PubMed  Google Scholar 

  98. Neu, C. P., M. L. Hull, J. H. Walton, and M. H. Buonocore. MRI-based technique for determining nonuniform deformations throughout the volume of articular cartilage explants. Magn. Reson. Med. 53:321–328, 2005.

    Article  CAS  PubMed  Google Scholar 

  99. Neu, C. P., A. Khalafi, K. Komvopoulos, T. M. Schmid, and A. H. Reddi. Mechanotransduction of bovine articular cartilage superficial zone protein by transforming growth factor beta signaling. Arthritis Rheum. 56:3706–3714, 2007.

    Article  CAS  PubMed  Google Scholar 

  100. Neu, C. P., A. H. Reddi, K. Komvopoulos, T. M. Schmid, and P. E. Di Cesare. Increased friction coefficient and superficial zone protein expression in patients with advanced osteoarthritis. Arthritis Rheum. 62:2680–2687, 2010.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Neu, C. P., and J. H. Walton. Displacement encoding for the measurement of cartilage deformation. Magn. Reson. Med. 59:149–155, 2007.

    Article  Google Scholar 

  102. Nguyen, T. M., B. Arnal, S. Song, Z. Huang, R. K. Wang, and M. O’Donnell. Shear wave elastography using amplitude-modulated acoustic radiation force and phase-sensitive optical coherence tomography. J. Biomed. Opt. 20:016001, 2015.

    Article  PubMed  PubMed Central  Google Scholar 

  103. Nguyen, T. M., J. F. Aubry, M. Fink, J. Bercoff, and M. Tanter. In vivo evidence of porcine cornea anisotropy using supersonic shear wave imaging. Invest. Ophthalmol. Vis. Sci. 55:7545–7552, 2014.

    Article  PubMed  Google Scholar 

  104. Nguyen, T. M., J. F. Aubry, D. Touboul, M. Fink, J. L. Gennisson, J. Bercoff, and M. Tanter. Monitoring of cornea elastic properties changes during UV-A/riboflavin-induced corneal collagen cross-linking using supersonic shear wave imaging: a pilot study. Invest. Ophthalmol. Vis. Sci. 53:5948–5954, 2012.

    Article  CAS  PubMed  Google Scholar 

  105. 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 

  106. Nightingale, K., M. S. Soo, R. Nightingale, and G. Trahey. Acoustic radiation force impulse imaging: in vivo demonstration of clinical feasibility. Ultrasound Med. Biol. 28:227–235, 2002.

    Article  PubMed  Google Scholar 

  107. O’Connell, G. D., E. J. Vresilovic, and D. M. Elliott. Human intervertebral disc internal strain in compression: the effect of disc region, loading position, and degeneration. J. Orthop. Res. 29:547–555, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  108. Oldenburg, A. L., and S. A. Boppart. Resonant acoustic spectroscopy of soft tissues using embedded magnetomotive nanotransducers and optical coherence tomography. Phys. Med. Biol. 55:1189–1201, 2010.

    Article  PubMed  PubMed Central  Google Scholar 

  109. Oldenburg, A. L., G. Wu, D. Spivak, F. Tsui, A. S. Wolberg, and T. H. Fischer. Imaging and elastometry of blood clots using magnetomotive optical coherence tomography and labeled platelets. IEEE J. Sel. Top. Quantum Electron. 18:1100–1109, 2012.

    Article  CAS  Google Scholar 

  110. Oliphant, T. E., A. Manduca, R. L. Ehman, and J. F. Greenleaf. Complex-valued stiffness reconstruction for magnetic resonance elastography by algebraic inversion of the differential equation. Magn. Reson. Med. 45:299–310, 2001.

    Article  CAS  PubMed  Google Scholar 

  111. Ophir, J., S. K. Alam, B. S. Garra, F. Kallel, E. E. Konofagou, T. Krouskop, C. R. B. Merritt, R. Righetti, R. Souchon, S. Srinivasan, and T. Varghese. Elastography: imaging the elastic properties of soft tissues with ultrasound. J. Med. Ultrason. 29:155–171, 2002.

    Article  Google Scholar 

  112. Ophir, J., S. K. Alam, B. Garra, F. Kallel, E. Konofagou, T. Krouskop, and T. Varghese. Elastography: ultrasonic estimation and imaging of the elastic properties of tissues. Proc. Inst. Mech. Eng. [H] 213:203–233, 1999.

    Article  CAS  Google Scholar 

  113. Ophir, J., I. Cespedes, H. Ponnekanti, Y. Yazdi, and X. Li. Elastography: a quantitative method for imaging the elasticity of biological tissues. Ultrason. Imaging 13:111–134, 1991.

    Article  CAS  PubMed  Google Scholar 

  114. Ophir, J., R. K. Miller, H. Ponnekanti, I. Cespedes, and A. D. Whittaker. Elastography of beef muscle. Meat Sci. 36:239–250, 1994.

    Article  CAS  PubMed  Google Scholar 

  115. Othman, S. F., E. T. Curtis, S. A. Plautz, A. K. Pannier, S. D. Butler, and H. Xu. MR elastography monitoring of tissue-engineered constructs. NMR Biomed. 25:452–463, 2012.

    Article  PubMed  Google Scholar 

  116. Othman S., M. Stosich, H. Xu, N. Marion, J. Mao and R. Magin. Monitoring adipogenesis in tissue-engineered fat in vitro using microscopic magnetic resonance elastography. In: International Society for Magnetic Resonance in Medicine, Seattle, USA, 2006.

  117. Othman, S. F., H. H. Xu, T. J. Royston, and R. L. Magin. Microscopic magnetic resonance elastography (mu MRE). Magn. Reson. Med. 54:605–615, 2005.

    Article  PubMed  Google Scholar 

  118. Othman S. F., H. H. Xu, T. J. Royston and R. L. Magin. Microscopic magnetic resonance elastography (mu MRE) applications. In: Medical Imaging 2005: Physiology, Function, and Structure From Medical Images, Pts 1 and 2, edited by A. A. Amini and A. Manduca, 2005, pp. 314–322.

  119. Özkaya N., M. Nordin, D. Goldsheyder and D. Leger. Statics: systems in equilibrium. In: Fundamentals of BiomechanicsSpringer Science + Business Media, 2012, p. 35–59.

  120. Paietta, R. C., S. E. Campbell, and V. L. Ferguson. Influences of spherical tip radius, contact depth, and contact area on nanoindentation properties of bone. J. Biomech. 44:285–290, 2011.

    Article  PubMed  Google Scholar 

  121. Palmeri, M. L., and K. R. Nightingale. On the thermal effects associated with radiation force imaging of soft tissue. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 51:551–565, 2004.

    Article  PubMed  Google Scholar 

  122. Palmeri, M. L., A. C. Sharma, R. R. Bouchard, R. W. Nightingale, and K. R. Nightingale. A finite-element method model of soft tissue response to impulsive acoustic radiation force. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 52:1699–1712, 2005.

    Article  PubMed  PubMed Central  Google Scholar 

  123. 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 

  124. 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 

  125. Parker, K. J., L. Gao, R. M. Lerner, and S. F. Levinson. Techniques for elastic imaging: a review. IEEE Eng. Med. Biol. Mag. 15:52–59, 1996.

    Article  Google Scholar 

  126. Ponnekanti, H., J. Ophir, and I. Cespedes. Axial stress distributions between coaxial compressors in elastography: an analytical model. Ultrasound Med. Biol. 18:667–673, 1992.

    Article  CAS  PubMed  Google Scholar 

  127. Provenzano, P. P., D. R. Inman, K. W. Eliceiri, and P. J. Keely. Matrix density-induced mechanoregulation of breast cell phenotype, signaling and gene expression through a FAK–ERK linkage. Oncogene 28:4326–4343, 2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Qi, W., R. Li, T. Ma, J. Li, K. Kirk Shung, Z. Chen, and K. Kirk Shung. Resonant acoustic radiation force optical coherence elastography. Appl. Phys. Lett. 103:103704, 2013.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  129. Qin, E. C., R. Sinkus, G. Q. Geng, S. Cheng, M. Green, C. D. Rae, and L. E. Bilston. Combining MR elastography and diffusion tensor imaging for the assessment of anisotropic mechanical properties: a phantom study. J. Magn. Reson. Imaging 37:217–226, 2013.

    Article  PubMed  Google Scholar 

  130. Razani, M., T. W. H. Luk, A. Mariampillai, P. Siegler, T.-R. Kiehl, M. C. Kolios, and V. X. D. Yang. Optical coherence tomography detection of shear wave propagation in inhomogeneous tissue equivalent phantoms and ex vivo carotid artery samples. Biomed. Opt. Express 5:895, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  131. Rogowska, J. Optical coherence tomographic elastography technique for measuring deformation and strain of atherosclerotic tissues. Heart 90:556–562, 2004.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  132. Sarvazyan, A. Mechanical imaging: a new technology for medical diagnostics. Int. J. Med. Inf. 49:195–216, 1998.

    Article  CAS  Google Scholar 

  133. 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 

  134. Scarcelli, G., P. Kim, and S. H. Yun. In vivo measurement of age-related stiffening in the crystalline lens by Brillouin optical microscopy. Biophys. J. 101:1539–1545, 2011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Scarcelli, G., and S. H. Yun. Confocal Brillouin microscopy for three-dimensional mechanical imaging. Nat. Photonics 2:39–43, 2008.

    Article  CAS  Google Scholar 

  136. Schmitt, J. OCT elastography: imaging microscopic deformation and strain of tissue. Opt. Express 3:199–211, 1998.

    Article  CAS  PubMed  Google Scholar 

  137. Schoen, F. J. Cardiac valves and valvular pathology: update on function, disease, repair, and replacement. Cardiovasc. Pathol. 14:189–194, 2005.

    Article  PubMed  Google Scholar 

  138. Shih, C. C., C. C. Huang, Q. Zhou, and K. K. Shung. High-resolution acoustic-radiation-force-impulse imaging for assessing corneal sclerosis. IEEE Trans. Med. Imaging 32:1316–1324, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  139. Song, S., Z. Huang, T. M. Nguyen, E. Y. Wong, B. Arnal, M. O’Donnell, and R. K. Wang. Shear modulus imaging by direct visualization of propagating shear waves with phase-sensitive optical coherence tomography. J. Biomed. Opt. 18:121509, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  140. Thitaikumar, A., L. M. Mobbs, C. M. Kraemer-Chant, B. S. Garra, and J. Ophir. Breast tumor classification using axial shear strain elastography: a feasibility study. Phys. Med. Biol. 53:4809–4823, 2008.

    Article  PubMed  Google Scholar 

  141. Thittai, A. K., J. M. Yamal, L. M. Mobbs, C. M. Kraemer-Chant, S. Chekuri, B. S. Garra, and J. Ophir. Axial-shear strain elastography for breast lesion classification: further results from in vivo data. Ultrasound Med. Biol. 37:189–197, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  142. Tomasek, J. J., G. Gabbiani, B. Hinz, C. Chaponnier, and R. A. Brown. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat. Rev. Mol. Cell Biol. 3:349–363, 2002.

    Article  CAS  PubMed  Google Scholar 

  143. Tripathy S., K. Takanari, R. Hashizume, Y. Hong, N. Amoroso, K. Fujimoto, M. Sacks, W. Wagner and K. Kim. In-vivo mechanical property assessment of a biodegradable polyurethane tissue construct on rat abdominal repair model using ultrasound elasticity imaging. In: Ultrasonics Symposium (IUS), 2010 IEEEIEEE, 2010, p. 1137–1140.

  144. Twa, M. D., J. Li, S. Vantipalli, M. Singh, S. Aglyamov, S. Emelianov, and K. V. Larin. Spatial characterization of corneal biomechanical properties with optical coherence elastography after UV cross-linking. Biomed. Opt. Express 5:1419–1427, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  145. Urs, R., H. O. Lloyd, and R. H. Silverman. Acoustic radiation force for noninvasive evaluation of corneal biomechanical changes induced by cross-linking therapy. J. Ultrasound Med. 33:1417–1426, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  146. Varghese, T. Quasi-static ultrasound elastography. Ultrasound Clin. 4:323–338, 2009.

    Article  PubMed  PubMed Central  Google Scholar 

  147. Varghese, T., E. E. Konofagou, J. Ophir, S. K. Alam, and M. Bilgen. Direct strain estimation in elastography using spectral cross-correlation. Ultrasound Med. Biol. 26:1525–1537, 2000.

    Article  CAS  PubMed  Google Scholar 

  148. Venkatesh, S. K., M. Yin, J. F. Glockner, N. Takahashi, P. A. Araoz, J. A. Talwalkar, and R. L. Ehman. Magnetic resonance elastography of liver tumors-preliminary results. AJR Am. J. Roentgenol. 190:1534, 2008.

    Article  PubMed  PubMed Central  Google Scholar 

  149. Wang, Y. X., Y. P. Huang, A. J. Liu, W. B. Wan, and Y. P. Zheng. An ultrasound biomicroscopic and water jet ultrasound indentation method for detecting the degenerative changes of articular cartilage in a rabbit model of progressive osteoarthritis. Ultrasound Med. Biol. 40:1296–1306, 2014.

    Article  PubMed  Google Scholar 

  150. Wang, S., and K. V. Larin. Noncontact depth-resolved micro-scale optical coherence elastography of the cornea. Biomed. Opt. Express 5:3807–3821, 2014.

    Article  PubMed  PubMed Central  Google Scholar 

  151. Wang, S., and K. V. Larin. Shear wave imaging optical coherence tomography (SWI-OCT) for ocular tissue biomechanics. Opt. Lett. 39:41–44, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  152. Wang, S., J. Li, R. K. Manapuram, F. M. Menodiado, D. R. Ingram, M. D. Twa, A. J. Lazar, D. C. Lev, R. E. Pollock, and K. V. Larin. Noncontact measurement of elasticity for the detection of soft-tissue tumors using phase-sensitive optical coherence tomography combined with a focused air-puff system. Opt. Lett. 37:5184, 2012.

    Article  PubMed  PubMed Central  Google Scholar 

  153. Wellman, P. S., E. P. Dalton, D. Krag, K. A. Kern, and R. D. Howe. Tactile imaging of breast masses: first clinical report. Arch. Surg. 136:204–208, 2001.

    Article  CAS  PubMed  Google Scholar 

  154. Wells, P. N. T., and H. D. Liang. Medical ultrasound: imaging of soft tissue strain and elasticity. J. R. Soc. Interface 8:1521–1549, 2011.

    Article  PubMed  PubMed Central  Google Scholar 

  155. Xu, L., Y. Lin, J. Han, Z. Xi, H. Shen, and P. Gao. Magnetic resonance elastography of brain tumors: preliminary results. Acta Radiol. 48:327–330, 2007.

    Article  CAS  PubMed  Google Scholar 

  156. Xu, H., S. F. Othman, L. Hong, I. A. Peptan, and R. L. Magin. Magnetic resonance microscopy for monitoring osteogenesis in tissue-engineered construct in vitro. Phys. Med. Biol. 51:719–732, 2006.

    Article  PubMed  Google Scholar 

  157. Yanagisawa, O., M. Niitsu, T. Kurihara, and T. Fukubayashi. Evaluation of human muscle hardness after dynamic exercise with ultrasound real-time tissue elastography: a feasibility study. Clin. Radiol. 66:815–819, 2011.

    Article  CAS  PubMed  Google Scholar 

  158. Yasar T. K., T. J. Royston and R. L. Magin. Taking MR elastography (MRE) to the microscopic scale (μMRE). In: Proceedings of Biomedical Imaging: from Nano to Macro, 2011 IEEE International Symposium, 2011, pp. 1618–1623.

  159. Yasar, T. K., T. J. Royston, and R. L. Magin. Wideband MR elastography for viscoelasticity model identification. Magn. Reson. Med. 70:479–489, 2013.

    Article  PubMed  PubMed Central  Google Scholar 

  160. Yeh, W.-C., P.-C. Li, Y.-M. Jeng, H.-C. Hsu, P.-L. Kuo, M.-L. Li, P.-M. Yang, and P. H. Lee. Elastic modulus measurements of human liver and correlation with pathology. Ultrasound Med. Biol. 28:467–474, 2002.

    Article  PubMed  Google Scholar 

  161. Yin, Z. Y., T. M. Schmid, T. K. Yasar, Y. F. Liu, T. J. Royston, and R. L. Magin. Mechanical characterization of tissue-engineered cartilage using microscopic magnetic resonance elastography. Tissue Eng. Part C-Methods 20:611–619, 2014.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  162. 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 

  163. Yue W., G. A. Steven, A. B. Stephen and F. I. Michael. Ultrasound and optical methods for dynamic viscoelastic imaging. In: Handbook of Imaging in Biological Mechanics, CRC Press, 2014, pp. 83–96.

  164. Zhang, X., Y. Yin, Y. Guo, N. Fan, H. Lin, F. Liu, X. Diao, C. Dong, X. Chen, T. Wang, and S. Chen. Measurement of quantitative viscoelasticity of bovine corneas based on lamb wave dispersion properties. Ultrasound Med. Biol. 41:1461–1472, 2015.

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported in part by NIH grants R01 AR063712 and R21 AR066230, and NSF grant CMMI 1100554.

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Authors and Affiliations

  1. Weldon School of Biomedical Engineering, Purdue University, West Lafayette, IN, 47907, USA

    Woong Kim & Corey P. Neu

  2. Department of Mechanical Engineering, University of Colorado, Boulder, CO, 80304, USA

    Virginia L. Ferguson, Mark Borden & Corey P. Neu

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Kim, W., Ferguson, V.L., Borden, M. et al. Application of Elastography for the Noninvasive Assessment of Biomechanics in Engineered Biomaterials and Tissues. Ann Biomed Eng 44, 705–724 (2016). https://doi.org/10.1007/s10439-015-1542-x

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