On the Destruction of Cancer Cells Using Laser-Induced Shock Waves: A Review on Experiments and Multiscale Computer Simulations
DOI:
https://doi.org/10.17140/ROJ-1-110Keywords:
Shock waves, Molecular dynamics, Multiscale Modeling, Computer simulations, Cancer cells, Ultrasound, Laser ablation, Drug deliveryAbstract
In the clinical treatment of solid tumors, besides traditional surgery and chemotherapy, the use
of High Intensity Focused Ultrasound (HIFU) has been established as a minimally non-invasive
technique for tumor treatment, which is based on coagulative necrosis of cells, induced by
conversion of mechanical energy into heat. Another, less developed technique for the destruction
or damage of tumor cells, is based on the pure mechanical effects of strong shock waves
on cells, which are generated by using laser ablation, thus avoiding the heat-related unwanted
side-effect when using HIFU (cutaneous burns of healthy tissue). Despite the general therapeutic
success of extracorporeal shock wave therapy in medicine, e.g. for disintegrating congrements,
the mechanical effects of shock waves on the cytoskeleton of cells, on the transient
permeability and rupture of cell membranes, or on tissue damage remain widely unknown. The
mechanical behavior of bio-macromolecules however, is of particular importance on the cellular
level as several basic and yet unanswered questions are raised: How are cell stresses and
energy transmitted through cells and in what way are the forces and interactions that determine
the stability of cell plasma membranes affected by a shock wave and give rise to cell deformation,
structural damage or rupture of the membrane with subsequent apoptosis? Here, we intend
to review research on the shock wave destruction of tumor cells and discuss the use of laserablation
as a new potential technique for tumor treatment. We also discuss here recent progress
in computational modeling strategies and techniques for understanding the basic physical
mechanisms that occur in the interaction of shock waves with cellular structures and show how
computer modeling and numerical simulation can contribute to a fundamental understanding
in this emerging multidisciplinary field, where physics, chemistry, biology and medicine meet.
References
Mendelsohn J, Howley PM, Israel MA, Gray JW, Thompson CB. The Molecular Basis of Cancer. Philadelphia, PA, USA: Elsevier Science; 2014.
Blagosklonny MV, Robey R, Bates S, Fojo T. Pretreatment with DNA-damaging agents permits selective killing of checkpoint-deficient cells by microtubule-active drugs. J Clin Invest. 2000; 105(4): 533-539. doi: 10.1172/JCI8625
Pearson OH, Manni A, Arafah BM. Antiestrogen treatment of breast cancer: An overview. Cancer Res. 1982; 42(8 Suppl): 3424s-3429s. Web site. http://cancerres.aacrjournals.org/content/42/8_Supplement/3424s.short. Accessed July 24, 2016
Suresh S. Biomechanics and biophysics of cancer cells. Acta Biomater. 2007; 3(4): 413-438. doi: 10.1016/j.actbio.2007.04. 002
Guck J, Schinkinger S, Lincoln B, et al. Optical deformability as an inherent cell marker for testing malignant transformation and metastatic competence. Biophys J. 2005; 88(5): 3689-3698. doi: 10.1529/biophysj.104.045476
Fuh G, Cunningham BC, Fukunaga R, Nagata S, Goeddel DV, Wells JA. Rational design of potent antagonists to the human growth hormone receptor. Science. 1992; 256(5064): 1677- 1680. doi: 10.1126/science.256.5064.1677
Gardel ML, Valentine MT, Crocker JC, Bausch AR, Weitz DA. Microrheology of entangled F-actin solutions. Phys Rev Lett. 2003; 91(15): 158302-158302. doi: 10.1103/PhysRevLett. 91.158302
Gardel ML, Schneider IC, Aratyn-Schaus Y, Waterman CM. Mechanical integration of actin and adhesion dynamics in cell migration. Annu Rev Cell Devel Biol. 2009; 26: 315-333. doi: 10.1146/annurev.cellbio.011209.122036
Dunn BB. Cancer: Solving an age-old problem. Nature. 2012; 483(7387): S2-S6. doi: 10.1038/483S2a
Lackey L, Peterson C, Barr RG. Contrast-enhanced ultrasound-guided radiofrequency ablation of renal tumors. Ultrasound Q. 2012; 28(4): 269-274. doi: 10.1097/RUQ.0b01 3e318274de66
Goyal J, Verma P, Sidana A, Georgiades CS, Rodriguez R. Single center comparative oncologic outcomes of surgical and percutaneous cryoablation for treatment of renal tumors. J Endourol. 2012; 26(11): 1413-1419. doi: 10.1089/end.2012.0244 RADIOLOGY
Vogl TJ, Straub R, Eichler K, Söllner O, Mack MG. Colorectal carcinoma metastases in liver: Laser-induced interstitial thermotherapy-local tumor control rate and survival data. Radiology. 2004; 230(2): 450-458. doi: 10.1148/radiol.2302020646
Suhr F, Delhasse Y, Bungartz G, Schmidt A, Pfannkuche K, Bloch W. Cell biological effects of mechanical stimulations generated by focused extracorporeal shock wave applications on cultured human bone marrow stromal cells. Stem Cell Res. 2013; 11(2): 951-964. doi: 10.1016/j.scr.2013.05.010
Carome EF, Clark NA, Moeller CE. Generation of acoustic signals in liquids by ruby laser-induced thermal stress transients. Appl Phys Lett. 1964; 4(6): 95-97. doi: 10.1063/1.1753985
Krehl POK. History of Shock Waves, Explosions and Impact: A Chronological and Biographical Reference. Berlin, Germany: Springer; 2009.
Steinhauser MO, Hiermaier S. A review of computational methods in materials science: Examples from shock-wave and polymer physics. Int Mol Sci. 2009; 10(12): 5135-5216. doi: 10.3390/ijms10125135
Rodriguez V, Saurel R, Jourdan G, Houas L. Solid-particle jet formation under shock-wave acceleration. Phys Rev E Stat Nonlin Soft Matter Phys. 2013; 88(6): 063011. doi: 10.1103/PhysRevE.88.063011
Zheng J, Chen QF, Gu YJ, Chen ZY. Hugoniot measurements of double-shocked precompressed dense xenon plasmas. Phys Rev E Stat Nonlin Soft Matter Phys. 2012; 86(6): 066406. doi: 10.1103/PhysRevE.86.066406
Falk K, Regan SP, Vorberger J, et al. Comparison between x-ray scattering and velocity-interferometry measurements from shocked liquid deuterium. Phys Rev E Stat Nonlin Soft Matter Phys. 2013; 87(4): 043112. doi: 10.1103/PhysRevE.87.043112
Brujan EA, Ikeda T, Matsumoto Y. Jet formation and shock wave emission during collapse of ultrasound-induced cavitation bubbles and their role in the therapeutic applications of high-intensity focused ultrasound. Phys Med Biol. 2005; 50(20): 4797- 4809. doi: 10.1088/0031-9155/50/20/004
Iakovlev S, Iakovlev S, Buchner C, et al. Resonance-like phenomena in a submerged cylindrical shell subjected to two consecutive shock waves: The effect of the inner fluid. J Fluids Struct. 2014; 50: 153-170. doi: 10.1016/j.jfluidstructs.2014.05.013
Bringa EM, Caro A, Wang YM, et al. Ultrahigh strength in nanocrystalline materials under shock loading. Science. 2005; 309(5742): 1838-1841. doi: 10.1126/science.1116723
Kadau K, Germann TC, Lomdahl PS, et al. Shock waves in polycrystalline iron. Phys Rev Lett. 2007; 98(13): 135701. doi: 10.1103/PhysRevLett.98.135701
Knudson MD, Desjarlais MP, Dolan DH. Shock-wave exploration of the high-pressure phases of carbon. Science. 2008; 322(5909): 1822-1825. doi: 10.1126/science.1165278
Gurnett DA, Kurth WS. Electron plasma oscillations upstream of the solar wind termination shock. Science. 2005; 309(5743): 2025-2027. doi: 10.1126/science.1117425
Gurnett DA, Kurth WS. Intense plasma waves at and near the solar wind termination shock. Nature. 2008; 454(7200): 78- 80. doi: 10.1038/nature07023
Dutton Z, Budde M, Slowe C, Hau LV. Observation of quantum shock waves created with ultra-compressed slow light pulses in a Bose-Einstein condensate. Science. 2001; 293(5530): 663-668. doi: 10.1126/science.1062527
Damski B. Shock waves in a one-dimensional Bose gas: From a Bose-Einstein condensate to a Tonks gas. Phys Rev A. 2006; 73(4): 043601. doi: 10.1103/physreva.73.043601
Chang JJ, Engels P, Hoefer MA. Formation of dispersive shock waves by merging and splitting Bose-Einstein condensates. Phys Rev Lett. 2008; 101(17): 170404. doi: 10.1103/PhysRevLett.101.170404
Millot M, Dubrovinskaia N, Černok A, et al. Planetary science. Shock compression of stishovite and melting of silica at planetary interior conditions. Science. 2015; 347(6220): 418- 420. doi: 10.1126/science.1261507
McKee CF, Draine BT. Interstellar shock waves. Science. 1991; 252(5004): 397-403. doi: 10.1126/science.252.5004.397
McClure S, Dorfmüller C. Extracorporeal shock wave therapy: Theory and equipment. Clin Tech Equine Pract. 2002; 2(4): 348-357. doi: 10.1053/j.ctep.2004.04.008
Lingeman JE, McAteer JA, Gnessin E, Evan AP. Shock wave lithotripsy: Advances in technology and technique. Nat Rev Urol. 2009; 6(12): 660-670. doi: 10.1038/nrurol.2009.216
Cherenkov PA. Visible emission of clean liquids by action of gamma radiation. R Dokl Akad Nauk SSSR. 1934; 2: 451-454. doi: 10.1234/12345678
Rassweiler JJ, Knoll T, Kohrmann KU, et al. Shock wave technology and application: An update. Eur Urol. 2011; 59(5): 784-796. doi: 10.1016/j.eururo.2011.02.033
Coleman AJ, Saunders JE. A review of the physical properRADIOLOGY ties and biological effects of the high amplitude acoustic fields used in extracorporeal lithotripsy. Ultrasonics. 1993; 31(2): 75- 89. doi: 10.1016/0041-624X(93)90037-Z
McAteer JA, Evan AP. The acute and long-term adverse effects of shock wave lithotripsy. Semin Nephrol. 2008; 28(2): 200-213. doi: 10.1016/j.semnephrol.2008.01.003
Brümmer F, Bräuner T, Hülser DF. Biological effects of shock waves. World J Urol. 1990; 8(4): 224-232. doi: 10.1007/BF01580025
Delius M. Medical applications and bioeffects of extracorporeal shock waves. Shock Waves. 1994; 4(2): 55-72. doi: 10.1007/BF01418569
Oosterhof GO, Smits GA, De Ruyter AE, Schalken JA, Debruyne FM. Effects of high-energy shock waves combined with biological response modifiers in different human kidney cancer xenografts. Ultrasound Med Biol. 1991; 17(4): 391-399. doi: 10.1016/0301-5629(91)90139-N
Gamarra F, Spelsberg F, Dellian M, Goetz AE. Complete local tumor remission after therapy with extra-corporeally applied high-energy shock waves (HESW). Int J Cancer. 1993; 55(1): 153-156. doi: 10.1002/ijc.2910550127
Lauer U, Bürgelt E, Squire Z, et al. Shock wave permeabilization as a new gene transfer method. Gene Ther. 1997; 4(7): 710-715. doi: 10.1038/sj.gt.3300462
Bao S, Thrall BD, Gies RA, Miller DL. In vivo transfection of melanoma cells by lithotripter shock waves. Cancer Res. 1998; 58(2): 219-221. Web site. http://cancerres.aacrjournals. org/content/58/2/219.short. Accessed July 24, 2016
Delius M, Adams G. Shock wave permeabilization with ribosome inactivating proteins: A new approach to tumor therapy. Cancer Res. 1999; 59(20): 5227-5232. Web site. http://cancerres.aacrjournals.org/content/59/20/5227.long. Accessed July 24, 2016
Tschoep K, Hartmann G, Jox R, et al. Shock waves: A novel method for cytoplasmic delivery of antisense oligonucleotides. J Mol Med. 2001; 79(5-6): 306-313. doi: 10.1007/s001090100204
Kodama T, Doukas AG, Hamblin MR. Delivery of ribosome-inactivating protein toxin into cancer cells with shock waves. Cancer Lett. 2003; 189(1): 69-75. doi: 10.1016/S0304- 3835(02)00503-7
Michel MS, Erben P, Trojan L, et al. Acoustic energy: a new transfection method for cancer of the prostate, cancer of the bladder and benign kidney cells. Anticancer Res. 2004; 24(4): 2303- 2308. Web site. http://ar.iiarjournals.org/content/24/4/2303. long. Accessed July 24, 2016
Ohl C-D, Wolfrum B. Detachment and sonoporation of adherent HeLa-cells by shock wave-induced cavitation. Biochim Biophys Acta. 2003; 1624(1-3): 131-138. doi: 10.1016/j.bbagen.2003.10.005
Ohl C-D, Arora M, Ikink R, et al. Sonoporation from jetting cavitation bubbles. Biophys J. 2006; 91(11): 4285-4295. doi: 10.1529/biophysj.105.075366
Moosavi-Nejad SF, Hosseini SMR, Satoh M, Takayama K. Shock wave induced cytoskeletal and morphological deformations in a human renal carcinoma cell line. Cancer Sci. 2006; 97(4): 296-304. doi: 10.1111/j.1349-7006.2006.00172.x
Bushnell JC, McCloskey DJ. Thermoelastic stress production in solids. J Appl Phys. 1968; 39(12): 5541-5546. doi: 10.1063/1.1656010
Yang LC. Stress waves generated in thin metallic films by a Q-switched ruby laser. 1974; 45(6): 2601-2608. doi: 10.1063/1.1663636
Fabbro R, Fournier J, Ballard P, Devaux D, Virmont J. Physical study of laser-produced plasma in confined geometry. J Appl Phys. 1990; 68(2): 775-784. doi: 10.1063/1.346783
Venugopalan V, Deutsch TF. Stress generated in polyimide by excimer-laser irradiation. J Appl Phys. 1993; 74(6): 4181- 4189. doi: 10.1063/1.354422
Doukas AG, Flotte TJ. Physical characteristics and biological effects of laser-induced stress waves. Ultrasound Med Biol. 1996; 22(2): 151-164. doi: 10.1016/0301-5629(95)02026-8
Yao C-P, Zhang Z-X, Rahmanzadeh R, Huettmann G. Laserbased gene transfection and gene therapy. IEEE Trans Nanobiosci. 2008; 7(2): 111-119. doi: 10.1109/TNB.2008.2000742
Doukas AG, Kollias N. Transdermal drug delivery with a pressure wave. Adv Drug Deliver Rev. 2004; 56(5): 559-579. doi: 10.1016/j.addr.2003.10.031
Brümmer F, Brenner J, Bräuner T, Hülser DF. Effect of shock waves on suspended and immobilized L1210 cells. Ultrasound Med Biol. 1989; 15(3): 229-239. doi: 10.1016/0301- 5629(89)90067-7
de Reijke TM, Schamhart DH, Kurth KH, Löwik CW, Donkers LH, Sterenborg HJ. Tumor growth delay by laser-generated shock waves. Lasers Surg Med. 1994; 14(3): 205-212. doi: 10.1002/lsm.1900140302
Doukas AG, McAuliffe DJ, Lee S, Venugopalan V, Flotte RADIOLOGY TJ. Physical factors involved in stress-wave-induced cell injury: The effect of stress gradient. Ultrasound Med Biol. 1995; 21(7): 961-967. doi: 10.1016/0301-5629(95)00027-O
Lee S, Anderson T, Zhang H, Flotte TJ, Doukas AG. Alteration of cell membrane by stress waves in vitro. Ultrasound Med Biol. 1996; 22(9): 1285-1293. doi: 10.1016/S0301- 5629(96)00149-4
Douki T, Lee S, Dorey K, Flotte TJ, Deutsch TF, Doukas AG. Stress-wave-induced injury to retinal pigment epithelium cells in vitro. Lasers Surg Med. 1996; 19(3): 249-259. doi: 10.1002/(SICI)1096-9101(1996)19:3<249::AID-LSM1>3.0.CO;2-S
Huber PE, Jenne J, Debus JJ, Wannenmacher MF, Pfisterer P. A comparison of shock wave and sinusoidal-focused ultrasound-induced localized transfection of HeLa cells. Ultrasound Med Biol. 1999; 25(9): 1451-1457. doi: 10.1016/S0301- 5629(99)00099-X
Kohri K, Uemura T, Iguchi M, Kurita T. Effect of high energy shock waves on tumor cells. Urol Res. 1990; 18(2): 101-105. doi: 10.1007/BF00302468
Mulholland SE, Lee S, McAuliffe DJ, Doukas AG. Cell loading with laser-generated stress waves: The role of the stress gradient. Pharm Res. 1999; 16(4): 514-518. doi: 10.1023/A:1018814911497
Lee S, Doukas AG. Laser-generated stress waves and their effects on the cell membrane. IEEE J Sel Top Quant. 1999; 5(4): 997-1003. doi: 10.1109/2944.796322
Kato M, Ioritani N, Suzuki T, et al. Mechanism of anti-tumor effect of combination of bleomycin and shock waves. Jpn J Cancer Res. 2000; 91(10): 1065-1072. doi: 10.1111/j.1349- 7006.2000.tb00886.x
Sondén A, Svensson B, Roman N, Brismar B, Palmblad J, Kjellstöm BT. Mechanisms of shock wave induced endothelial cell injury. Lasers Surg Med. 2002; 31(4): 233-241. doi: 10.1002/lsm.10093
Kodama T, Kodama T, Hamblin MR, Hamblin MR, Doukas AG. Cytoplasmic molecular delivery with shock waves: Importance of impulse. Biophys J. 2000; 79(4): 1821-1832. doi: 10.1016/S0006-3495(00)76432-0
Juhasz T, Hu XH, Turi L, Bor Z. Dynamics of shock waves and cavitation bubbles generated by picosecond laser pulses in corneal tissue and water. Lasers Surg Med. 1993; 15(1): 91-98. doi: 10.1002/lsm.1900150112
Strand OT, Goosman DR, Martinez C, Whitworth TL, Kuhlow WW. Compact system for high-speed velocimetry using heterodyne techniques. Rev Sci Instrum. 2006; 77(8): 083108. doi: 10.1063/1.2336749
Schmidt M, Kahlert U, Wessolleck J, et al. Characterization of a setup to test the impact of high-amplitude pressure waves on living cells. Nature Sci Rep. 2014; 4: 3849. doi: 10.1038/srep03849
Steinhauser MO, Steinhauser MO, Schmidt M. Destruction of cancer cells by laser-induced shock waves: Recent developments in experimental treatments and multiscale computer simulations. Soft Matter. 2014; 10(27): 4778-4788. doi: 10.1039/c4sm00407h
Fung YC. Biomechanics: Motion, Flow, Stress, and Growth. New York, USA: Springer; 1990.
Verdier C. Rheological Properties of Living Materials. From Cells to Tissues. J Theoretical Medicine. 2003; 5(2): 67-91. doi: 10.1080/10273360410001678083
de Gennes PG. Scaling Concepts in Polymer Physics. Ithaca, London, UK; Cornell University Press; 1979.
Steinhauser MO. Computational Multiscale Modeling of Fluids and Solids - Theory and Applications. 2nd ed. New York, USA: Springer; 2016.
Steinhauser MO. A molecular dynamics study on universal properties of polymer chains in different solvent qualities. Part I. A review of linear chain properties. J Chem Phys. 2005; 122(9): 094901. doi: 10.1063/1.1846651
Bienfait Y. Modelling and molecular dynamics simulations of flexible polymer networks. In: Steinhauser MO, ed. December 2013.
Schindler T, Kröner D, Steinhauser MO. On the dynamics of molecular self-assembly and the structural analysis of bilayer membranes using coarse-grained molecular dynamics simulations. Biochim Biophys Acta. 2016; 1858(9): 1955-1963. doi: 10.1016/j.bbamem.2016.05.014
Doi M, Edwards SF. The Theory of Polymer Dynamics. New york, USA: Clarendon Press, Oxford; 1986.
Bird RB, Hassager O, Armstrong RC, Curtis CF. Dynamics of Polymeric Liquids. New York, USA: Wiley; 1977.
Larson RG. The Structure and Rheology of Complex Fluids. New York, USA: Oxford University Press; 1999.
Winter HH. Analysis of linear viscoelasticity of a crosslinking polymer at the gel point. J Rheol. 1986; 30(2): 367. doi: 10.1122/1.549853 RADIOLOGY
Flory PJ. Statistical Mechanics of Chain Molecules. New Jersey, USA: John Wiley & Sons, Inc; 1969.
Einstein A. Eine neue Bestimmung der Moleküldimensionen. Ann Phys. 1906; 324(2): 289-306. doi: 10.1002/andp. 19063240204
Oldroyd JG. The elastic and viscous properties of emulsions and suspensions. Science. 1953; 218(1132): 122-132. doi: 10.1098/rspa.1953.0092
Hashin Z, Rosen BW. The elastic moduli of fiber-reinforced materials. J Appl Mech. 1964; 31(2): 223-232. doi: 10.1115/1.3629590
Hill CR. Theory of mechanical properties of fibre-strengthened materials: I. Elastic behaviour. J Mech Phys Solids. 1964; 12(4): 199-212. doi: 10.1016/0022-5096(64)90019-5
Fung YC. Microrheology and constitutive equation of soft tissue. Biorheology. 1988; 25(1-2): 261-270. Web site. http:// europepmc.org/abstract/med/3196823. Accessed July 24, 2016
Choy TC. Effective Medium Theory: Principles and Applications. Oxford, UK: Oxford University Press; 1999.
Ingber DE, Heidemann SR, Lamoureux P, Buxbaum RE. Opposing views on tensegrity as a structural framework for understanding cell mechanics. J Appl Physiol. 2000; 89(4): 1663- 1678. doi: 10.1016/0012-1606(71)90073-X
Stamenovic D, Ingber DE. Models of cytoskeletal mechanics of adherent cells. Biomech Model Mechan. 2002; 1(1): 95- 108. doi: 10.1007/s10237-002-0009-9
Ingber DE. Tensegrity I. Cell structure and hierarchical systems biology. J Cell Sci. 2003; 116(Pt 7): 1157-1173. doi: 10.1242/jcs.00359
Wang N, Naruse K, Stamenovic D, et al. Mechanical behavior in living cells consistent with the tensegrity model. Proc Natl Acad Sci. 2001; 98(14): 7765-7770. doi: 10.1073/pnas.141199598
Ingber DE, Wang N, Stamenovic D. Tensegrity, cellular biophysics, and the mechanics of living systems. Rep Prog Phys. 2014; 77(4): 046603. doi: 10.1088/0034-4885/77/4/046603
Pritchard RH, Huang YYS, Terentjev EM. Mechanics of biological networks: From the cell cytoskeleton to connective tissue. Soft Matter. 2014; 10(12): 1864-1884. doi: 10.1039/c3sm52769g
Ingber DE, Madri JA, Jamieson JD. Role of basal lamina in neoplastic disorganization of tissue architecture. PNAS. 1981; 78(6): 3901-3905. Web site. http://www.pnas.org/content/78/6/3901.short. Accessed July 24, 2016
Chen D, Wen Q, Janmey PA. Rheology of soft materials. Condensed Matter Physics. 2010; 1: 301-322. doi: 10.1146/annurev-conmatphys-070909-104120
Müller KW, Bruinsma RF, Lieleg O, Bausch AR, Wall WA, Levine AJ. Rheology of semiflexible bundle networks with transient linkers. Phys Rev Lett. 2014; 112(23): 238102-238102. doi: 10.1103/PhysRevLett.112.238102
Brunner C, Niendorf A, Käs JA. Passive and active singlecell biomechanics: A new perspective in cancer diagnosis. Soft Matter. 2009; 5(11): 2171-2178. doi: 10.1039/b807545j
Sayed El T, Mota A, Fraternali F, Ortiz M. A variational constitutive model for soft biological tissues. J Biomech. 2008; 41(7): 1458-1466. doi: 10.1016/j.jbiomech.2008.02.023
Qin Z, Dimas L, Adler D, Bratzel G, Buehler MJ. Biological materials by design. J Phys Condens Matter. 2014; 26(7): 073101. doi: 10.1088/0953-8984/26/7/073101
Meyers MA, Chen P-Y, Lopez MI, Seki Y, Lin AYM. Biological materials: A materials science approach. J Mech Behav Biomed. 2011; 4(5): 626-657. doi: 10.1016/j.jmbbm.2010.08.005
Ogden RW. Large Deformation Isotropic Elasticity - On the Correlation of Theory and Experiment for Incompressible Rubberlike Solids. Proceedings of the Royal Society of London A: Mathematical, Physical and Engineering Sciences. 1972; 326(1567): 565-584. doi: 10.1098/rspa.1972.0026
Mooney M. A theory of large elastic deformation. J Appl Phys. 1940; 11(9): 582-592. doi: 10.1063/1.1712836
Rivlin RS. Large Elastic Deformations of Isotropic Materials. IV. Further Developments of the General Theory. Philosophical Transactions of the Royal Society of London Series A Mathematical and Physical Sciences. 1948; 241(8): 379-397. doi: 10.1098/rsta.1948.0024
Miller K, Chinzei K. Mechanical properties of brain tissue in tension. J Biomech. 2002; 35(4): 483-490. doi: 10.1016/S0021-9290(01)00234-2
Xu M, Nowinski WL. Talairach-Tournoux brain atlas registration using a metalforming principle-based finite element method. Med Image Anal. 2001; 5(4): 271-279. doi: 10.1016/S1361-8415(01)00045-7
Warfield SK, Haker SJ, Talos I-F, et al. Capturing intraoperative deformations: research experience at Brigham and Women’s Hospital. Med Image Anal. 2005; 9(2): 145-162. doi: 10.1016/j.media.2004.11.005 RADIOLOGY
Miller K, Chinzei K. Constitutive modelling of brain tissue: Experiment and theory. J Biomech. 1997; 30(11-12): 1115-1121. doi: 10.1016/S0021-9290(97)00092-4
Miller K. Method of testing very soft biological tissues in compression. J Biomech. 2005; 38(1): 153-158. doi: 10.1016/j. jbiomech.2004.03.004
Wittek A, Kikinis R, Warfield SK, Miller K. Brain shift computation using a fully nonlinear biomechanical model. Med Image Comput Comput Assist Interv. 2005; 8(Pt 2): 583-590. doi: 10.1007/11566489_72
Wittek A, Hawkins T, Miller K. On the unimportance of constitutive models in computing brain deformation for imageguided surgery. Biomech Model Mechan. 2008; 8(1): 77-84. doi: 10.1007/s10237-008-0118-1
Dumpuri P, Thompson RC, Dawant BM, Cao A, Miga MI. An atlas-based method to compensate for brain shift: Preliminary results. Med Image Anal. 2007; 11(2): 128-145. doi: 10.1016/j.media.2006.11.002
Bathe KJ. Finite Element Procedures in Engineering Analysis. Cambridge, UK: Prentice Hall; 1982.
Cash DM, Miga MI, Sinha TK, Galloway RL, Chapman WC. Compensating for intraoperative soft-tissue deformations using incomplete surface data and finite elements. IEEE Trans Med Imaging. 2005; 24(11): 1479-1491. doi: 10.1109/TMI.2005.855434
Kim JS, Sun SX. Continuum modeling of forces in growing viscoelastic cytoskeletal networks. J Theor Biol. 2009; 256(4): 596-606. doi: 10.1016/j.jtbi.2008.10.023
Kim S-H, Suh HS, Cho MH, Lee SY, Kim T-S. Finite element simulation of ultrasound propagation in bone for quantitative ultrasound toward the diagnosis of osteoporosis. Conf Proc IEEE Eng Med Biol Soc. 2009; 2009: 436-439. doi: 10.1109/IEMBS.2009.5334707
Hostettler A, George D, Rémond Y, Nicolau SA, Soler L, Marescaux J. Bulk modulus and volume variation measurement of the liver and the kidneys in vivo using abdominal kinetics during free breathing. Comput Meth Prog Bio. 2010; 100(2): 149-157. doi: 10.1016/j.cmpb.2010.03.003
Cleveland RO, Lifshitz DA, Connors BA, Evan AP, Willis LR, Crum LA. In vivo pressure measurements of lithotripsy shock waves in pigs. Ultrasound Med Biol. 1998; 24(2): 293- 306. doi: 10.1016/S0301-5629(97)00270-6
Schwartz J-M, Denninger M, Rancourt D, Moisan C, Laurendeau D. Modelling liver tissue properties using a non-linear visco-elastic model for surgery simulation. Med Image Anal. 2005; 9(2): 103-112. doi: 10.1016/j.media.2004.11.002
Nava A, Mazza E, Kleinermann F, Avis NJ, McClure J. Determination of the mechanical properties of soft human tissues through aspiration experiments. Medical Image Computing and Computer-Assisted Intervention. 2003; 2003: 222-229. doi: 10.1007/978-3-540-39899-8_28
Ottensmeyer MP. Minimally invasive instrument for in vivo measurement of solid organ mechanical impedance. Web site. https://dspace.mit.edu/handle/1721.1/8858. Accessed July 24, 2016
Zhu Y, Dong Z, Wejinya UC, Jin S, Ye K. Determination of mechanical properties of soft tissue scaffolds by atomic force microscopy nanoindentation. J Biomech. 2011; 44(13): 2356- 2361. doi: 10.1016/j.jbiomech.2011.07.010
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