A three-dimensional in vitro tumor platform for modeling therapeutic irreversible electroporation

Biophysical Journal

Volumn 103, Issue 9, 2012, Pages 2033-2042

  Arena, Christopher B ^a   Szot, Christopher S ^a   Garcia, Paulo A ^a   Rylander, Marissa Nichole ^a   Davalos, Rafael V ^a  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLLAGEN TYPE 1;

ANIMAL; ARTICLE; CELL DEATH; ELECTROMAGNETIC FIELD; ELECTROPORATION; EXPERIMENTAL NEOPLASM; HYDROGEL; MOUSE; PHENOTYPE; TEMPERATURE; TUMOR CELL LINE;

ANIMALS; CELL DEATH; CELL LINE, TUMOR; COLLAGEN TYPE I; ELECTROMAGNETIC FIELDS; ELECTROPORATION; HYDROGELS; MICE; NEOPLASMS, EXPERIMENTAL; PHENOTYPE; TEMPERATURE;

EID: 84868525106     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2012.09.017     Document Type: Article

References (67)

1. R.V. Davalos, I.L. Mir, and B. Rubinsky Tissue ablation with irreversible electroporation Ann. Biomed. Eng. 33 2005 223 231
2. P.A. Garcia, and T. Pancotto R.V. Davalos Non-thermal irreversible electroporation (N-TIRE) and adjuvant fractionated radiotherapeutic multimodal therapy for intracranial malignant glioma in a canine patient Technol. Cancer Res. Treat. 10 2011 73 83
3. R.E. Neal 2nd, and J.H. Rossmeisl Jr. R.V. Davalos Successful treatment of a large soft tissue sarcoma with irreversible electroporation J. Clin. Oncol. 29 2011 e372 e377
4. K.R. Thomson, and W. Cheung A. Haydon Investigation of the safety of irreversible electroporation in humans J. Vasc. Interv. Radiol. 22 2011 611 621
5. S. Bagla, and D. Papadouris Percutaneous irreversible electroporation of surgically unresectable pancreatic cancer: a case report J. Vasc. Interv. Radiol. 23 2012 142 145
6. C. Ball, K.R. Thomson, and H. Kavnoudias Irreversible electroporation: a new challenge in "out of operating theater" anesthesia Anesth. Analg. 110 2010 1305 1309
7. T.P. Kingham, and A.M. Karkar Y. Fong Ablation of perivascular hepatic malignant tumors with irreversible electroporation J. Am. Coll. Surg. 215 2012 379 387
8. G. Onik, P. Mikus, and B. Rubinsky Irreversible electroporation: implications for prostate ablation Technol. Cancer Res. Treat. 6 2007 295 300
9. J.F. Edd, and L. Horowitz B. Rubinsky In vivo results of a new focal tissue ablation technique: irreversible electroporation IEEE Trans. Biomed. Eng. 53 2006 1409 1415
10. G. Onik, and B. Rubinsky Irreversible electroporation: first patient experience focal therapy of prostate cancer B. Rubinsky, Irreversible Electroporation 2010 Springer, Berlin/Heidelberg 235 247
11. E. Maor, A. Ivorra, and B. Rubinsky Non thermal irreversible electroporation: novel technology for vascular smooth muscle cells ablation PLoS ONE 4 2009 e4757
12. W. Li, and Q.Y. Fan Z. Li The effects of irreversible electroporation (IRE) on nerves PLoS ONE 6 2011 e18831
13. B. Rubinsky, G. Onik, and P. Mikus Irreversible electroporation: a new ablation modality - clinical implications Technol. Cancer Res. Treat. 6 2007 37 48
14. Y. Zhang, and Y. Guo A.C. Larson MR imaging to assess immediate response to irreversible electroporation for targeted ablation of liver tissues: preclinical feasibility studies in a rodent model Radiology 256 2010 424 432
15. E.W. Lee, and C. Chen S.T. Kee Advanced hepatic ablation technique for creating complete cell death: irreversible electroporation Radiology 255 2010 426 433
16. A. Deodhar, and S. Monette S.B. Solomon Percutaneous irreversible electroporation lung ablation: preliminary results in a porcine model Cardiovasc. Intervent. Radiol. 34 2011 1278 1287
17. L. Appelbaum, and E. Ben-David S.N. Goldberg US findings after irreversible electroporation ablation: radiologic-pathologic correlation Radiology 262 2012 117 125
18. E. Ben-David, and L. Appelbaum S.N. Goldberg Characterization of irreversible electroporation ablation in in vivo porcine liver AJR Am. J. Roentgenol. 198 2012 W62 W68
19. M. Bower, and L. Sherwood R. Martin Irreversible electroporation of the pancreas: definitive local therapy without systemic effects J. Surg. Oncol. 104 2011 22 28
20. K.P. Charpentier, and F. Wolf D.E. Dupuy Irreversible electroporation of the pancreas in swine: a pilot study HPB (Oxford) 12 2010 348 351
21. D. Miklavcic, and D. Semrov L.M. Mir A validated model of in vivo electric field distribution in tissues for electrochemotherapy and for DNA electrotransfer for gene therapy Biochim. Biophys. Acta 1523 2000 73 83
22. M.B. Sano, and R.E. Neal R.V. Davalos Towards the creation of decellularized organ constructs using irreversible electroporation and active mechanical perfusion Biomed. Eng. Online 9 2010 83
23. P.A. Garcia, and J.H. Rossmeisl Jr. R.V. Davalos Intracranial nonthermal irreversible electroporation: in vivo analysis J. Membr. Biol. 236 2010 127 136
24. R.E. Neal 2nd, and R. Singh R.V. Davalos Treatment of breast cancer through the application of irreversible electroporation using a novel minimally invasive single needle electrode Breast Cancer Res. Treat. 123 2010 295 301
25. D. Miklavcic, and D. Sel L. Mir Sequential finite element model of tissue electropermeabilisation Conf. Proc. IEEE Eng. Med. Biol. Soc. 5 2004 3551 3554
26. A. Ivorra, and B. Rubinsky In vivo electrical impedance measurements during and after electroporation of rat liver Bioelectrochemistry 70 2007 287 295
27. N. Pavselj, and Z. Bregar D. Miklavcic The course of tissue permeabilization studied on a mathematical model of a subcutaneous tumor in small animals IEEE Trans. Biomed. Eng. 52 2005 1373 1381
28. P.A. Garcia, and J.H. Rossmeisl Jr. R.V. Davalos A parametric study delineating irreversible electroporation from thermal damage based on a minimally invasive intracranial procedure Biomed. Eng. Online 10 2011 34
29. R.E. Neal 2nd, and P.A. Garcia R.V. Davalos Experimental characterization and numerical modeling of tissue electrical conductivity during pulsed electric fields for irreversible electroporation treatment planning IEEE Trans. Biomed. Eng. 59 2012 1076 1085
30. A. Ivorra, and B. Al-Sakere L.M. Mir In vivo electrical conductivity measurements during and after tumor electroporation: conductivity changes reflect the treatment outcome Phys. Med. Biol. 54 2009 5949 5963
31. R.E. Neal 2nd, and R.V. Davalos The feasibility of irreversible electroporation for the treatment of breast cancer and other heterogeneous systems Ann. Biomed. Eng. 37 2009 2615 2625
32. L. Miller, J. Leor, and B. Rubinsky Cancer cells ablation with irreversible electroporation Technol. Cancer Res. Treat. 4 2005 699 705
33. H. Shafiee, P.A. Garcia, and R.V. Davalos A preliminary study to delineate irreversible electroporation from thermal damage using the Arrhenius equation J. Biomech. Eng. 131 2009 074509
34. A. Ivorra, L.M. Mir, and B. Rubinsky Electric field redistribution due to conductivity changes during tissue electroporation: experiments with a simple vegetal model IFMBE Proc. 25 2010 59 62
35. M. Hjouj, and B. Rubinsky Magnetic resonance imaging characteristics of nonthermal irreversible electroporation in vegetable tissue J. Membr. Biol. 236 2010 137 146
36. K.M. Yamada, and E. Cukierman Modeling tissue morphogenesis and cancer in 3D Cell 130 2007 601 610
37. J.B. Kim Three-dimensional tissue culture models in cancer biology Semin. Cancer Biol. 15 2005 365 377
38. L.G. Griffith, and M.A. Swartz Capturing complex 3D tissue physiology in vitro Nat. Rev. Mol. Cell Biol. 7 2006 211 224
39. C. Fischbach, and R. Chen D.J. Mooney Engineering tumors with 3D scaffolds Nat. Methods 4 2007 855 860
40. C.S. Szot, and C.F. Buchanan M.N. Rylander 3D in vitro bioengineered tumors based on collagen I hydrogels Biomaterials 32 2011 7905 7912
41. S.S. Verbridge, and N.W. Choi C. Fischbach Oxygen-controlled three-dimensional cultures to analyze tumor angiogenesis Tissue Eng. Part A 16 2010 2133 2141
42. J. von Burstin, and S. Eser D. Saur E-cadherin regulates metastasis of pancreatic cancer in vivo and is suppressed by a SNAIL/HDAC1/HDAC2 repressor complex Gastroenterology 137 2009 361 371 371, e1-e5
43. B. Seidler, and A. Schmidt D. Saur A Cre-loxP-based mouse model for conditional somatic gene expression and knockdown in vivo by using avian retroviral vectors Proc. Natl. Acad. Sci. USA 105 2008 10137 10142
44. D. Saur, and B. Seidler R.M. Schmid CXCR4 expression increases liver and lung metastasis in a mouse model of pancreatic cancer Gastroenterology 129 2005 1237 1250
45. M.J. Paszek, and N. Zahir V.M. Weaver Tensional homeostasis and the malignant phenotype Cancer Cell 8 2005 241 254
46. B. Al-Sakere, and F. André L.M. Mir Tumor ablation with irreversible electroporation PLoS ONE 2 2007 e1135
47. N. Pavselj, and D. Miklavcic Resistive heating and electropermeabilization of skin tissue during in vivo electroporation: a coupled nonlinear finite element model Int. J. Heat Mass Transf 54 2011 2294 2302
48. J.F. Edd, and R.V. Davalos Mathematical modeling of irreversible electroporation for treatment planning Technol. Cancer Res. Treat. 6 2007 275 286
49. M. Pavlin, T. Slivnik, and D. Miklavcic Effective conductivity of cell suspensions IEEE Trans. Biomed. Eng. 49 2002 77 80
50. C. Polk, and E. Postow Handbook of Biological Effects of Electromagnetic Fields 1996 CRC Press Boca Raton, FL
51. H.P. Schwan, and K.R. Foster Rf-field interactions with biological systems: electrical properties and biophysical mechanisms Proc. IEEE 68 1980 104 113
52. C.B. Arena, and M.B. Sano R.V. Davalos High-frequency irreversible electroporation (H-FIRE) for non-thermal ablation without muscle contraction Biomed. Eng. Online 10 2011 102
53. C. Kanthou, and S. Kranjc M. Cemazar The endothelial cytoskeleton as a target of electroporation-based therapies Mol. Cancer Ther. 5 2006 3145 3152
54. A.J. Chapman Fundamentals of Heat Transfer 1987 Macmillan London
55. L. Bozec, and M. Odlyha Thermal denaturation studies of collagen by microthermal analysis and atomic force microscopy Biophys. J. 101 2011 228 236
56. J. Belehradek Jr., and S. Orlowski L.M. Mir Electropermeabilization of cells in tissues assessed by the qualitative and quantitative electroloading of bleomycin Biochim. Biophys. Acta 1190 1994 155 163
57. S. Haberl, and M. Pavlin Use of collagen gel as a three-dimensional in vitro model to study electropermeabilization and gene electrotransfer J. Membr. Biol. 236 2010 87 95
58. J.W. Henshaw, and F. Yuan Field distribution and DNA transport in solid tumors during electric field-mediated gene delivery J. Pharm. Sci. 97 2008 691 711
59. M.A. dit Faute, and L. Laurent H. Bobichon Distinctive alterations of invasiveness, drug resistance and cell-cell organization in 3D-cultures of MCF-7, a human breast cancer cell line, and its multidrug resistant variant Clin. Exp. Metastasis 19 2002 161 168
60. B. St Croix, and V.A. Florenes R.S. Kerbel Impact of the cyclin-dependent kinase inhibitor p27Kip1 on resistance of tumor cells to anticancer agents Nat. Med. 2 1996 1204 1210
61. J. Lee, and G.D. Lilly N.A. Kotov In vitro toxicity testing of nanoparticles in 3D cell culture Small 5 2009 1213 1221
62. E.D. Kirson, and V. Dbalý Y. Palti Alternating electric fields arrest cell proliferation in animal tumor models and human brain tumors Proc. Natl. Acad. Sci. USA 104 2007 10152 10157
63. H.P. Schwan Electrical properties of tissue and cell suspensions Adv. Biol. Med. Phys. 5 1957 147 209
64. R.V. Davalos, and D.M. Otten B. Rubinsky Electrical impedance tomography for imaging tissue electroporation IEEE Trans. Biomed. Eng. 51 2004 761 767
65. M.E. Mezeme, and G. Pucihar D. Miklavcic A numerical analysis of multicellular environment for modeling tissue electroporation Appl. Phys. Lett. 100 2012 143701 143705
66. Reference deleted in proof.
67. J. Chiu, and P.G. Fair Determination of thermal conductivity by differential scanning calorimetry Thermochim. Acta 34 1979 267 273