Thermal ablation of tumours: Biological mechanisms and advances in therapy

Nature Reviews Cancer

Volumn 14, Issue 3, 2014, Pages 199-208

  Chu, Katrina F ^a   Dupuy, Damian E ^a  

^a RHODE ISLAND HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABLATION TECHNIQUES; ANIMALS; APOPTOSIS; HISTORY, 19TH CENTURY; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; HUMANS; NEOPLASMS; SURGERY, COMPUTER-ASSISTED;

EID: 84894562122     PISSN: 1474175X     EISSN: 14741768     Source Type: Journal    
DOI: 10.1038/nrc3672     Document Type: Review

References (118)

1. Tiong, L. & Maddern, G. J. Systematic review and meta-analysis of survival and disease recurrence after radiofrequency ablation for hepatocellular carcinoma. Br. J. Surg. 98, 1210-1224 (2011).
2. Ahmed, M., Brace, C. L., Lee, F. T. & Goldberg, S. N. Principles of and advances in percutaneous ablation. Radiology 258, 351-369 (2011).
3. Pereira, P. L. Actual role of radiofrequency ablation of liver metastases. Eur. Radiol. 17, 2062-2070 (2007).
4. Paulet, E. et al. Factors limiting complete tumor ablation by radiofrequency ablation. Cardiovasc. Interv. Radiol. 31, 107-115 (2008).
5. Haen, S. P., Pereira, P. L., Salih, H. R., Rammensee, H.-G. & Gouttefangeas, C. More than just tumor destruction: immunomodulation by thermal ablation of cancer. Clin. Dev. Immunol. 2011, 1-19 (2011).
6. Kwan, K. G. & Matsumoto, E. D. Radiofrequency ablation and cryoablation of renal tumours. Curr. Oncol. 14, 34-38 (2007).
7. Davalos, R. V., Mir, L. M. & Rubinsky, B. Tissue ablation with irreversible electroporation. Ann. Biomed. Eng. 33, 223-231 (2005).
8. Sánchez-Ortiz, R. F., Tannir, N., Ahrar, K. & Wood, C. G. Spontaneous regression of pulmonary metastases from renal cell carcinoma after radio frequency ablation of primary tumor: an in situ tumor vaccine? J. Urol. 170, 178-179 (2003).
9. Kim, H., Park, B. K. & Kim, C. K. Spontaneous regression of pulmonary and adrenal metastases following percutaneous radiofrequency ablation of a recurrent renal cell carcinoma. Kor. J. Radiol. 9, 470-472 (2008).
10. Soanes, W. A., Ablin, R. J. & Gonder, M. J. Remission of metastatic lesions following cryosurgery in prostatic cancer: immunologic considerations. J. Urol. 104, 154-159 (1970).
11. McGahan, J. P. et al. Hepatic ablation with use of radio-frequency electrocautery in the animal model. J. Vasc. Interv. Radiol. 3, 291-297 (1992).
12. Formenti, S. C. & Demaria, S. Systemic effects of local radiotherapy. Lancet Oncol. 10, 718-726 (2009).
13. Nikfarjam, M., Muralidharan, V. & Christophi, C. Mechanisms of focal heat destruction of liver tumors. J. Surg. Res. 127, 208-223 (2005).
14. Fajardo, L. F., Egbert, B., Marmor, J. & Hahn, G. M. Effects of hyperthermia in a malignant tumor. Cancer 45, 613-623 (1980).
15. Willis, W. T., Jackman, M. R., Bizeau, M. E., Pagliassotti, M. J. & Hazel, J. R. Hyperthermia impairs liver mitochondrial function in vitro. Am. J. Physiol. 278, R1240-R1246 (2000).
16. Wheatley, D. N., Kerr, C. & Gregory, D. W. Heatinduced damage to HeLa-S3 cells: correlation of viability, permeability, osmosensitivity, phase-contrast light-, scanning electron-and transmission electronmicroscopical findings. Int. J. Hyperthermia. 5, 145-162 (1989).
17. Warters, R. L. & Roti Roti, J. L. Hyperthermia and the Cell Nucleus. Radiat. Res. 92, 458-462 (1982).
18. Dupuy, D. E. et al. Radiofrequency ablation followed by conventional radiotherapy for medically inoperable stage I non-small cell lung cancer. Chest 129, 738-745 (2006).
19. Hines-Peralta, A. et al. Improved tumor destruction with arsenic trioxide and radiofrequency ablation in three animal models. Radiology 240, 82-89 (2006).
20. Wright, A. S., Sampson, L. A., Warner, T. F., Mahvi, D. M. & Lee, F. T. Radiofrequency versus microwave ablation in a hepatic porcine model. Radiology 236, 132-139 (2005).
21. Muralidharan, V., Malcontenti-Wilson, C. & Christophi, C. Effect of blood flow occlusion on laser hyperthermia for liver metastases. J. Surg. Res. 103, 165-174 (2002).
22. Whelan, W. M., Wyman, D. R. & Wilson, B. C. Investigations of large vessel cooling during interstitial laser heating. Med. Phys. 22, 105-115 (1995).
23. Dromi, S. A. et al. Radiofrequency ablation induces antigen-presenting cell infiltration and amplification of weak tumor-induced immunity. Radiology 251, 58-66 (2009).
24. Wissniowski, T. T. et al. Activation of tumor-specific T lymphocytes by radio-frequency ablation of the VX2 hepatoma in rabbits. Cancer Res. 63, 6496-6500 (2003).
25. Zerbini, A. et al. Radiofrequency thermal ablation for hepatocellular carcinoma stimulates autologous NK-cell response. Gastroenterology 138, 1931-1942 (2010).
26. Nijkamp, M. W. et al. Radiofrequency ablation of colorectal liver metastases induces an inflammatory response in distant hepatic metastases but not in local accelerated outgrowth. J. Surg. Oncol. 101, 551-556 (2010).
27. Rughetti, A. et al. Modulation of blood circulating immune cells by radiofrequency tumor ablation. J. Exp. Clin. Cancer Res. 22, 247-250 (2003).
28. Ali, M. Y. et al. Activation of dendritic cells by local ablation of hepatocellular carcinoma. J. Hepatol. 43, 817-822 (2005).
29. Fietta, A. M. et al. Systemic inflammatory response and downmodulation of peripheral CD25+Foxp3+ T-regulatory cells in patients undergoing radiofrequency thermal ablation for lung cancer. Hum. Immunol. 70, 477-486 (2009).
30. den Brok, M. H. M. G. M. et al. In situ tumor ablation creates an antigen source for the generation of antitumor immunity. Cancer Res. 64, 4024-4029 (2004).
31. Sabel, M. S. Cryo-immunology: a review of the literature and proposed mechanisms for stimulatory versus suppressive immune responses. Cryobiology 58, 1-11 (2009).
32. Erinjeri, J. P. et al. Image-guided thermal ablation of tumors increases the plasma level of Interleukin-6 and Interleukin-10. J. Vasc. Interv. Radiol. 24, 1105-1112 (2013).
33. Ahmad, F. et al. Changes in interleukin-1ß and 6 after hepatic microwave tissue ablation compared with radiofrequency, cryotherapy and surgical resections. Am. J. Surg. 200, 500-506 (2010).
34. Teng, L.-S., Jin, K.-T., Han, N. & Cao, J. Radiofrequency ablation, heat shock protein 70 and potential antitumor immunity in hepatic and pancreatic cancers: a minireview. Hepatobiliary Pancreat. Dis. Int. 9, 361-365 (2010).
35. Schueller, G. et al. Heat shock protein expression induced by percutaneous radiofrequency ablation of hepatocellular carcinoma in vivo. Int. J. Oncol. 24, 609-613 (2004).
36. Rai, R. et al. Study of apoptosis and heat shock protein (HSP) expression in hepatocytes following radiofrequency ablation (RFA). J. Surg. Res. 129, 147-151 (2005).
37. Solazzo, S. A. et al. Liposomal doxorubicin increases radiofrequency ablation-induced tumor destruction by increasing cellular oxidative and nitrative and stress accelerating apoptotic pathways. Radiology. 255, 62-74 (2010).
38. Yang, W.-L. et al. Heat shock protein 70 is induced in mouse human colon tumor xenografts after sublethal radiofrequency ablation. Ann. Surg. Oncol. 11, 399-406 (2004).
39. Basu, S., Binder, R. J., Suto, R., Anderson, K. M. & Srivastava, P. K. Necrotic but not apoptotic cell death releases heat shock proteins, which deliver a partial maturation signal to dendritic cells and activate the NF-.B pathway. Int. Immunol. 12, 1539-1546 (2000).
40. Garrido, C., Brunet, M., Didelot, C., Schmitt, E. & Kroemer, G. Heat shock proteins 27 and 70: antiapoptotic proteins with tumorigenic properties. Cell Cycle 5, 2592-2601 (2006).
41. Chen, T., Guo, J., Han, C., Yang, M. & Cao, X. Heat shock protein 70, released from heat-stressed tumor cells, initiates antitumor immunity by inducing tumor cell chemokine production and activating dendritic cells via TLR4 pathway. J. Immunol. 182, 1449-1459 (2009).
42. Figueiredo, C. et al. Heat shock protein 70 (HSP70) induces cytotoxicity of T-helper cells. Blood 113, 3008-3016 (2009).
43. den Brok, M. H. M. G. M. et al. Efficient loading of dendritic cells following cryo and radiofrequency ablation in combination with immune modulation induces anti-tumour immunity. Br. J. Cancer 95, 896-905 (2006).
44. Arnold, D., Faath, S., Rammensee, H. & Schild, H. Cross-priming of minor histocompatibility antigenspecific cytotoxic T cells upon immunization with the heat shock protein gp96. J. Exp. Med. 182, 885-889 (1995).
45. Srivastava, P. Interaction of heat shock proteins with peptides and antigen presenting cells: chaperoning of the innate and adaptive immune responses. Annu. Rev. Immunol. 20, 395-425 (2002).
46. Haen, S. P. et al. Elevated serum levels of heat shock protein 70 can be detected after radiofrequency ablation. Cell Stress Chaperones 16, 495-504 (2011).
47. Schueller, G. et al. Expression of heat shock proteins in human hepatocellular carcinoma after radiofrequency ablation in an animal model. Oncol. Rep. 12, 495-499 (2004).
48. Hiroishi, K. et al. Strong CD8+ T-cell responses against tumor-associated antigens prolong the recurrence-free interval after tumor treatment in patients with hepatocellular carcinoma. J. Gastroenterol. 45, 451-458 (2010).
49. Lubner, M. G., Brace, C. L., Hinshaw, J. L. & Lee, F. T. Microwave tumor ablation: mechanism of action, clinical results and devices. J. Vasc. Interv. Radiol. 21, S192-S203 (2010).
50. Wright, A. S., Lee, F. T. & Mahvi, D. M. Hepatic microwave ablation with multiple antennae results in synergistically larger zones of coagulation necrosis. Ann. Surg. Oncol. 10, 275-283 (2003).
51. Ahmad, F. et al. Renal effects of microwave ablation compared with radiofrequency, cryotherapy and surgical resection at different volumes of the liver treated. Liver Int. 30, 1305-1314 (2010).
52. Dong, B. W. et al. Sequential pathological and immunologic analysis of percutaneous microwave coagulation therapy of hepatocellular carcinoma. Int. J. Hyperthermia. 19, 119-133 (2003).
53. Mala, T. Cryoablation of liver tumours-a review of mechanisms, techniques and clinical outcome. Minim. Invasive Ther. Allied Technol. 15, 9-17 (2006).
54. Mala, T. et al. Magnetic resonance imaging-estimated three-dimensional temperature distribution in liver cryolesions: a study of cryolesion characteristics assumed necessary for tumor ablation. Cryobiology 43, 268-275 (2001).
55. Hoffmann, N. E. & Bischof, J. C. The cryobiology of cryosurgical injury. Urology 60, 40-49 (2002).
56. Lovelock, J. E. The haemolysis of human red bloodcells by freezing and thawing. Biochim. Biophys. Acta. 10, 414-426 (1953).
57. Baust, J. G. & Gage, A. A. The molecular basis of cryosurgery. BJU Int. 95, 1187-1191 (2005).
58. Hanai, A., Yang, W. L. & Ravikumar, T. S. Induction of apoptosis in human colon carcinoma cells HT29 by sublethal cryo-injury: mediation by cytochrome c release. Int. J. Cancer 93, 526-533 (2001).
59. Yang, W.-L., Addona, T., Nair, D. G., Qi, L. & Ravikumar, T. S. Apoptosis induced by cryo-injury in human colorectal cancer cells is associated with mitochondrial dysfunction. Int. J. Cancer 103, 360-369 (2003).
60. Alblin, R. J., Soanes, W. A. & Gonder, M. J. Prospects for cryo-immunotherapy in cases of metastasizing carcinoma of the prostate. Cryobiology 8, 271-279 (1971).
61. Gursel, E., Roberts, M. & Veenema, R. J. Regression of prostatic cancer following sequential cryotherapy to the prostate. J. Urol. 108, 928-932 (1972).
62. Ablin, R. J. Cryosurgery of the rabbit prostate. Comparison of the immune response of immature and mature bucks. Cryobiology 11, 416-422 (1974).
63. Ablin, R. et al. Cryosurgery of the monkey (macaque) prostate. I. Humoral immunologic responsiveness following cryostimulation. Cryobiology 13, 47-53 (1976).
64. Ablin, R. J. & Reddy, K. P. Cryosurgery of the monkey (macaque) prostate. II. Apparent immunopathologic alterations following cryostimulation. Cryobiology 14, 205-214 (1977).
65. Jansen, M. C. et al. Cryoablation induces greater inflammatory and coagulative responses than radiofrequency ablation or laser induced thermotherapy in a rat liver model. Surgery 147, 686-695 (2010).
66. Chapman, W. C. et al. Hepatic cryoablation, but not radiofrequency ablation, results in lung inflammation. Ann. Surg. 231, 752-761 (2000).
67. Ravindranath, M. H. et al. Cryosurgical ablation of liver tumors in colon cancer patients increases the serum total ganglioside level and then selectively augments antiganglioside IgM. Cryobiology 45, 10-21 (2002).
68. Gravante, G., Sconocchia, G., Ong, S. L., Dennison, A. R. & Lloyd, D. M. Immunoregulatory effects of liver ablation therapies for the treatment of primary and metastatic liver malignancies. Liver Int. 29, 18-24 (2009).
69. Chapman, W. C. et al. Hepatic cryoablation-induced acute lung injury. Arch. Surg. 135, 667-673 (2013).
70. Blackwell, T. S. et al. Acute lung injury after hepatic cryoablation: correlation with NF-.B activation and cytokine production. Surgery 126, 518-526 (1999).
71. Gazzaniga, S. et al. Inflammatory changes after cryosurgery-induced necrosis in human melanoma xenografted in nude mice. J. Invest. Dermatol. 116, 664-671 (2001).
72. Sabel, M. S. et al. Immunologic response to cryoablation of breast cancer. Breast Cancer Res. Treat. 90, 97-104 (2005).
73. Blackwood, C. E. & Cooper, I. S. Response of experimental tumor systems to cryosurgery. Cryobiology 9, 508-515 (1972).
74. Urano, M., Tanaka, C., Sugiyama, Y., Miya, K. & Saji, S. Antitumor effects of residual tumor after cryoablation: the combined effect of residual tumor and a proteinbound polysaccharide on multiple liver metastases in a murine model. Cryobiology 46, 238-245 (2003).
75. Gallucci, S., Lolkema, M. & Matzinger, P. Natural adjuvants: endogenous activators of dendritic cells. Nature Med. 5, 1249-1255 (1999).
76. Sauter, B. et al. Consequences of cell death: exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J. Exp. Med. 191, 423-434 (2000).
77. Seifert, J. K. et al. Large volume hepatic freezing: association with significant release of the cytokines interleukin-6 and tumor necrosis factor a in a rat model. World J. Surg. 26, 1333-1341 (2002).
78. Wing, M. G., Rogers, K., Jacob, G. & Rees, R. C. Characterisation of suppressor cells generated following cryosurgery of an HSV-2-induced fibrosarcoma. Cancer Immunol. Immunother. 26, 169-175 (1988).
79. Yamashita, T. et al. Enhanced tumor metastases in rats following cryosurgery of primary tumor. Gann 73, 222-228 (1982).
80. Sabel, M. S., Su, G., Griffith, K. A. & Chang, A. E. Rate of freeze alters the immunologic response after cryoablation of breast cancer. Ann. Surg. Oncol. 17, 1187-1193 (2010).
81. Yang, W. et al. Combination therapy of radiofrequency ablation and transarterial chemoembolization in recurrent hepatocellular carcinoma after hepatectomy compared with single treatment. Hepatol. Res. 39, 231-240 (2009).
82. Peng, Z.-W. et al. Radiofrequency ablation as first-line treatment for small solitary hepatocellular carcinoma: long-term results. Eur. J. Surg. Oncol. 36, 1054-1060 (2010).
83. Yang, P., Liang, M., Zhang, Y. & Shen, B. Clinical application of a combination therapy of lentinan, multi-electrode RFA and TACE in HCC. Adv. Ther. 25, 787-794 (2008).
84. Morimoto, M. et al. Midterm outcomes in patients with intermediate-sized hepatocellular carcinoma: a randomized controlled trial for determining the efficacy of radiofrequency ablation combined with transcatheter arterial chemoembolization. Cancer 116, 5452-5460 (2010).
85. Hakime, A. et al. Combination of radiofrequency ablation with antiangiogenic therapy for tumor ablation efficacy: study in mice. Radiology 244, 464-470 (2007).
86. Goldberg, S. N., Hahn, P. F., Halpern, E. F., Fogle, R. M. & Gazelle, G. S. Radio-frequency tissue ablation: effect of pharmacologic modulation of blood flow on coagulation diameter. Radiology 209, 761-767 (1998).
87. Horkan, C. et al. Radiofrequency ablation: effect of pharmacologic modulation of hepatic and renal blood flow on coagulation diameter in a VX2 tumor model. J. Vasc. Interv. Radiol. 15, 269-274 (2004).
88. Machlenkin, A. et al. Combined dendritic cell cryotherapy of tumor induces systemic antimetastatic immunity. Clin. Cancer Res. 11, 4955-4961 (2005).
89. den Brok, M. H. M. G. M. et al. Synergy between in situ cryoablation and TLR9 stimulation results in a highly effective in vivo dendritic cell vaccine. Cancer Res. 66, 7285-7292 (2006).
90. Redondo, P. et al. Imiquimod enhances the systemic immunity attained by local cryosurgery destruction of melanoma lesions. J. Invest. Dermatol. 127, 1673-1680 (2007).
91. Nierkens, S. et al. Route of administration of the TLR9 agonist CpG critically determines the efficacy of cancer immunotherapy in mice. PLoS ONE 4, e8368 (2009).
92. Waitz, R. et al. Potent induction of tumor immunity by combining tumor cryoablation with anti-CTLA-4 therapy. Cancer Res. 72, 430-439 (2012).
93. Sabel, M. S., Arora, A., Su, G. & Chang, A. E. Adoptive immunotherapy of breast cancer with lymph node cells primed by cryoablation of the primary tumor. Cryobiology 53, 360-366 (2006).
94. Yang, W. et al. Do liposomal apoptotic enhancers increase tumor coagulation and end-point survival in percutaneous radiofrequency ablation of tumors in a rat model? Radiology 257, 685-696 (2010).
95. Yang, W. et al. Radiofrequency ablation combined with liposomal quercetin to increase tumor destruction by modulation of heat shock protein production in a small animal model. Int. J. Hyperthermia 27, 527-538 (2011).
96. Goldberg, S. N. et al. Percutaneous tumor ablation: increased necrosis with combined radio-frequency ablation and intratumoral doxorubicin injection in a rat breast tumor model. Radiology 220, 420-427 (2001).
97. Goldberg, S. N. et al. Percutaneous tumor ablation: increased necrosis with combined radio-frequency ablation and intravenous liposomal doxorubicin in a rat breast tumor model. Radiology 222, 797-804 (2002).
98. Goldberg, S. N. et al. Radiofrequency ablation of hepatic tumors: increased tumor destruction with adjuvant liposomal doxorubicin therapy. AJR Am. J. Roentgenol. 179, 93-101 (2002).
99. Lasic, D. D. & Papahadjopoulos, D. Liposomes revisited. Science 267, 1275-1276 (1995).
100. Ranson, M., Howell, A., Cheeseman, S. & Margison, J. Liposomal drug delivery. Cancer Treat. Rev. 22, 366-379 (1996).
101. Chen, Q. et al. Tumor microvascular permeability is a key determinant for antivascular effects of doxorubicin encapsulated in a temperature sensitive liposome. Int. J. Hyperthermia 24, 475-482 (2008).
102. Kong, G. et al. Efficacy of liposomes and hyperthermia in a human tumor xenograft model: importance of triggered drug release. Cancer Res. 60, 6950-6957 (2000).
103. Poon, R. T. & Borys, N. Lyso-thermosensitive liposomal doxorubicin: an adjuvant to increase the cure rate of radiofrequency ablation in liver cancer. Futur. Oncol. 7, 937-945 (2011).
104. Solazzo, S. et al. RF ablation with adjuvant therapy: comparison of external beam radiation and liposomal doxorubicin on ablation efficacy in an animal tumor model. Int. J. Hyperthermia 24, 560-567 (2008).
105. Horkan, C. et al. Reduced tumor growth with combined radiofrequency ablation and radiation therapy in a rat breast tumor model. Radiology 235, 81-88 (2005).
106. Chan, M., Dupuy, D., Mayo-Smith, W., Ng, T. & DiPetrillo, T. Combined radiofrequency ablation and high-dose rate brachytherapy for early-stage nonsmall-cell lung cancer. Brachytherapy 10, 253-259 (2011).
107. Grieco, C. A. et al. Percutaneous image-guided thermal ablation and radiation therapy: outcomes of combined treatment for 41 patients with inoperable stage I/II non-small-cell lung cancer. J. Vasc. Interv. Radiol. 17, 1117-1124 (2006).
108. Onik, G., Mikus, P. & Rubinsky, B. Irreversible electroporation: implications for prostate ablation. Technol. Cancer Res. Treat. 6, 295-300 (2007).
109. Okino, M. & Mohri, H. Effects of a high-voltage electrical impulse and an anticancer drug on in vivo growing tumors. Jpn J. Cancer Res. 78, 1319-1321 (1987).
110. Rubinsky, B., Onik, G. & Mikus, P. Irreversible electroporation: a new ablation modality-clinical implications. Technol. Cancer Res. Treat. 6, 37-48 (2007).
111. Faroja, M. et al. Irreversible electroporation ablation: is all the damage nonthermal? Radiology 266, 462-470 (2013).
112. Srimathveeravalli, G. et al. Evaluation of an endorectal electrode for performing focused irreversible electroporation ablations in the swine rectum. J. Vasc. Interv. Radiol. 24, 1249-1256 (2013).
113. Palucka, K. & Banchereau, J. Cancer immunotherapy via dendritic cells. Nature Rev. Cancer 12, 265-277 (2013).
114. Hamamoto, S. et al. Radiofrequency ablation and immunostimulant OK-432: combination therapy enhances systemic antitumor immunity for treatment of VX2 lung tumors in rabbits. Radiology 267, 405-413 (2013).
115. Johnson, E. E. et al. Radiofrequency ablation combined with KS-IL2 immunocytokine (EMD 273066) results in an enhanced antitumor effect against murine colon adenocarcinoma. Clin. Cancer Res. 15, 4875-4884 (2009).
116. Bovie, W. T. & Cushing, H. Electrosurgery as an aid to the removal of intracranial tumors with a preliminary note on a new surgical-current generator. Surg. Gynecol. Obs. 47, 751-784 (1928).
117. Lynn, J. G., Zwemer, R. L., Chick, A. J. & Miller, A. E. A new method for the generation and use of focused ultrasound in experimental biology. J. Gen. Physiol. 26, 179-193 (1942).
118. Gage, A. A. & Baust, J. Mechanisms of tissue injury in cryosurgery. Cryobiology 37, 171-186 (1998)