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Heat-Based Tumor Ablation: Role of the Immune Response

Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 880)

Abstract

The ideal cancer therapy not only induces the death of all localized tumor cells with less damage to surrounding normal tissue, but also activates a systemic antitumor immunity. Heat-based tumor ablation has the potential to be such a treatment as it can minimal-invasively ablate a targeted tumor below the skin surface, and may subsequently augment host antitumor immunity. This chapter primarily introduces increasing pre-clinical and clinical evidence linking antitumor immune response to thermal tumor ablation, and then discusses the potential mechanisms involved in ablation-enhanced host antitumor immunity. The seminal studies performed so far indicate that although it is not possible to make definite conclusions on the connection between thermal ablation and antitumor immune response, it is nonetheless important to conduct extensive studies on the subject in order to elucidate the processes involved.

Keywords

Heat Ablation Neoplasm Thermal ablation Immunity High intensity focused ultrasound Radiofrequency Microwave Laser Cryoablation Antigen presenting cell Cytotoxic T lymphocyte Tumor infiltrating lymphocyte Heat shock protein Tumor vaccine 

References

  1. Adams DO, Hamilton TA (1984) The cell biology of macrophage activation. Annu Rev Immunol 2:283–318PubMedCrossRefGoogle Scholar
  2. Ali MY, Grimm CF, Ritter M, Mohr L, Allgaier HP, Weth R, Bocher WO, Endrulat K, Blum HE, Geissler M (2005) Activation of dendritic cells by local ablation of hepatocellular carcinoma. J Hepatol 43:817–822PubMedCrossRefGoogle Scholar
  3. Babaian RJ, Donnelly B, Bahn D, Baust JG, Dineen M, Ellis D, Katz A, Pisters L, Rukstalis D, Shinohara K, Thrasher JB (2008) Best practice statement on cryosurgery for the treatment of localized prostate cancer. J Urol 180:1993–2004PubMedCrossRefGoogle Scholar
  4. Barry MA, Behnke CA, Eastman A (1990) Activation of programmed cell death (apoptosis) by cisplatin, other anticancer drugs, toxins and hyperthermia. Biochem Pharmacol 40:2353–2362PubMedCrossRefGoogle Scholar
  5. Beland M, Mueller PR, Gervais DA (2007) Thermal ablation in interventional oncology. Semin Roentgenol 42:175–190PubMedCrossRefGoogle Scholar
  6. Benndorf R, Bielka H (1997) Cellular stress response: stress proteins – physiology and implications for cancer. Recent Results Cancer Res 143:129–144PubMedCrossRefGoogle Scholar
  7. Cabibbo G, Latteri F, Antonucci M, Craxì A (2009) Multimodal approaches to the treatment of hepatocellular carcinoma. Nat Clin Pract Gastroenterol Hepatol 6:159–169PubMedCrossRefGoogle Scholar
  8. Carrafiello G, Laganà D, Mangini M, Fontana F, Dionigi G, Boni L, Rovera F, Cuffari S, Fugazzola C (2008) Microwave tumors ablation: principles, clinical applications and review of preliminary experiences. Int J Surg 6:S65–S69PubMedCrossRefGoogle Scholar
  9. Chapman WC, Debelak JP, Blackwell TS, Gainer KA, Christman JW, Pinson CW, Brigham KL, Parker RE (2000a) Hepatic cryoablation, but not radiofrequency ablation, results in lung inflammation. Arch Surg 135:667–672PubMedCrossRefGoogle Scholar
  10. Chapman WC, Debelak JP, Blackwell TS, Gainer KA, Christman JW, Pinson CW, Brigham KL, Parker RE (2000b) Hepatic cryoablation-induced acute lung injury: pulmonary hemodynamic and permeability effects in a sheep model. Arch Surg 135:667–672PubMedCrossRefGoogle Scholar
  11. Chapman WC, Debelak JP, Wright Pinson C, Washington MK, Atkinson JB, Venkatakrishnan A, Blackwell TS, Christman JW (2000c) Hepatic cryoablation, but not radiofrequency ablation, results in lung inflammation. Ann Surg 231:752–761PubMedCentralPubMedCrossRefGoogle Scholar
  12. Chaussy C, Thuroff S, Rebillard X, Gelet A (2005) Technology insight: high-intensity focused ultrasound for urologic cancers. Nat Clin Pract Urol 2:191–198PubMedCrossRefGoogle Scholar
  13. Clement GT (2004) Perspectives in clinical uses of high-intensity focused ultrasound. Ultrasonics 42:1087–1093PubMedCrossRefGoogle Scholar
  14. Curley SA (2001) Radiofrequency ablation of malignant liver tumors. Oncologist 6:14–23PubMedCrossRefGoogle Scholar
  15. Decadt B, Siriwardena AK (2004) Radiofrequency ablation of liver tumours: systematic review. Lancet Oncol 5:550–560PubMedCrossRefGoogle Scholar
  16. Decker T, Lohmann-Matthes ML, Karck U, Peters T, Decker K (1989) Comparative study of cytotoxicity, tumor necrosis factor, and prostaglandin release after stimulation of rat Kupffer cells, murine Kupffer cells, and murine inflammatory liver macrophages. J Leukoc Biol 45:139–146PubMedGoogle Scholar
  17. den Brok MH, Sutmuller RP, van der Voort R, Bennink EJ, Figdor CG, Ruers TJ, Adema GJ (2004) In situ tumor ablation creates an antigen source for the generation of antitumor immunity. Cancer Res 64:4024–4029CrossRefGoogle Scholar
  18. den Brok MH, Sutmuller RP, Nierkens S, Bennink EJ, Frielink C, Toonen LW, Boerman OC, Figdor CG, Ruers TJ, Adema GJ (2006) Efficient loading of dendritic cells following cryo and radiofrequency ablation in combination with immune modulation induces antitumor immunity. Br J Cancer 95:896–905CrossRefGoogle Scholar
  19. Deng J, Zhang Y, Feng J, Wu F (2010) Dendritic cells loaded with ultrasound-ablated tumour induce in vivo specific antitumour immune responses. Ultrasound Med Biol 36:441–448PubMedCrossRefGoogle Scholar
  20. Dewey WC (1994) Arrhenius relationships from the molecule and cell to the clinic. Int J Hyperthermia 10:457–483PubMedCrossRefGoogle Scholar
  21. Diederich CJ, Hynynen K (1999) Ultrasound technology for hyperthermia. Ultrasound Med Biol 25:871–887PubMedCrossRefGoogle Scholar
  22. Dong B, Zhang J, Liang P, Yu X, Su L, Yu D, Ji X, Yu G, Yin Z (2002) Influencing factors of local immunocyte infiltration in hepatocellular carcinoma tissues pre-and post-percutaneous microwave coagulation therapy. Zhonghua Yi Xue Za Zhi 82:393–397PubMedGoogle Scholar
  23. Dong BW, Zhang J, Liang P, Yu XL, Su L, Yu DJ, Ji XL, Yu G (2003) Sequential pathological and immunologic of percutaneous microwave coagulation therapy of hepatocellular carcinoma. Int J Hyperthermia 19:119–133PubMedCrossRefGoogle Scholar
  24. Dromi SA, Walsh MP, Herby S, Traughber B, Xie J, Sharma KV, Sekhar KP, Luk A, Liewehr DJ, Dreher MR, Fry TJ, Wood BJ (2009) Radiofrequency ablation induces antigen-presenting cell infiltration and amplification of weak tumor-induced immunity. Radiology 251:58–66PubMedCentralPubMedCrossRefGoogle Scholar
  25. Dumot JA, Greenwald BD (2008) Argon plasma coagulation, bipolar cautery, and cryotherapy: ABC’s of ablative techniques. Endoscopy 40:1026–1032PubMedCrossRefGoogle Scholar
  26. Emami B, Song CW (1984) Physiological mechanisms in hyperthermia: a review. Int J Radiat Oncol Biol Phys 10:289–298PubMedCrossRefGoogle Scholar
  27. Evrard S, Menetrier-Caux C, Biota C, Neaud V, Mathoulin-Pélissier S, Blay JY, Rosenbaum J (2007) Cytokines pattern after surgical radiofrequency ablation of liver colorectal metastases. J Gastroenterol Clin Biol 31:141–145CrossRefGoogle Scholar
  28. Fagnoni FF, Zerbini A, Pelosi G, Missale G (2008) Combination of radiofrequency ablation and immunotherapy. Front Biosci 13:369–381PubMedCrossRefGoogle Scholar
  29. Fan Q, Ma B, Guo A, Li Y, Ye J, Zhou Y, Qiu X (1996) Surgical treatment of bone tumors in conjunction with microwave-induced hyperthermia and adjuvant immunotherapy. A preliminary report. Chin Med J 109:425–431PubMedGoogle Scholar
  30. Fesenko EE, Makar VR, Novoselova EG, Sadovnikov VB (1999) Microwaves and cellular immunity. I. Effect of whole body microwave irradiation on tumor necrosis factor production in mouse cells. Bioelectrochem Bioenerg 49:29–35PubMedCrossRefGoogle Scholar
  31. Fietta AM, Morosini M, Passadore I, Cascina A, Draghi P, Dore S, Rossi R, Pozzi E, Meloni F (2009) Systemic inflammatory response and downmodulation of peripheral CD25+ Foxp3+ T-regulatory cells in patients undergoing radiofrequency thermal ablation for lung cancer. Hum Immunol 70:477–486PubMedCrossRefGoogle Scholar
  32. Gallucci S, Lolkema M, Matzinger P (1999) Natural adjuvants: endogenous activators of dendritic cells. Nat Med 5:1249–1255PubMedCrossRefGoogle Scholar
  33. Germer CT, Roggan A, Ritz JP, Isbert C, Albrecht D, Muller G, Buhr HJ (1998a) Optical properties of native and coagulated human liver tissue and liver metastases in the near infrared range. Lasers Surg Med 23:194–203PubMedCrossRefGoogle Scholar
  34. Germer C, Isbert CM, Albrecht D, Ritz JP, Schilling A, Roggan A, Wolf KJ, Muller G, Buhr H (1998b) Laser-induced thermotherapy for the treatment of liver metastasis. Correlation of gadolinium-DTPA-enhanced MRI with histomorphologic findings to determine criteria for follow-up monitoring. Surg Endosc 12:1317–1325PubMedCrossRefGoogle Scholar
  35. Goldberg SN, Gazelle GS, Halpern EF, Rittman WJ, Mueller PR, Rosenthal DI (1996) Radiofrequency tissue ablation: importance of local temperature along the electrode tip exposure in determining lesion shape and size. Acad Radiol 3:212–218PubMedCrossRefGoogle Scholar
  36. Goldberg SN, Gazelle GS, Mueller PR (2000) Thermal ablation therapy for focal malignancy: a unified approach to underlying principles, techniques, and diagnostic imaging guidance. AJR Am J Roentgenol 174:323–331PubMedCrossRefGoogle Scholar
  37. Goldberg SN, Grassi CJ, Cardella JF, Charboneau JW, Dodd GD, Dupuy DE, Gervais D, Gillams AR, Kane RA, Lee FT, Livraghi T, McGahan J, Phillips DA, Rhim H, Silverman SG (2005) Image-guided tumor ablation: standardization of terminology and reporting criteria. Radiology 235:728–739PubMedCentralPubMedCrossRefGoogle Scholar
  38. Gough-Palmer AL, Gedroyc WM (2008) Laser ablation of hepatocellular carcinoma – a review. World J Gastroenterol 14:7170–7174PubMedCentralPubMedCrossRefGoogle Scholar
  39. Gravante G, Sconocchia G, Ong SL, Dennison AR, Lloyd DM (2009) Immunoregulatory effects of liver ablation therapies for the treatment of primary and metastatic liver malignancies. Liver Int 29:18–24PubMedCrossRefGoogle Scholar
  40. Habibi M, Kmieciak M, Graham L, Morales JK, Bear HD, Manjili MH (2009) Radiofrequency thermal ablation of breast tumors combined with intralesional administration of IL-7 and IL-15 augments anti-tumor immune responses and inhibits tumor development and metastasis. Breast Cancer Res Treat 114:423–431PubMedCentralPubMedCrossRefGoogle Scholar
  41. Hafron J, Kaouk JH (2007) Ablative techniques for the management of kidney cancer. Nat Clin Pract Urol 4:261–269PubMedCrossRefGoogle Scholar
  42. Han XJ, Dong BW, Liang P, Yu XL, Yu DJ (2009) Local cellular immune response induced by ultrasound-guided tumor bed superantigen injection after percutaneous microwave coagulation therapy for liver cancer. Zhonghua Zhong Liu Za Zhi 31:602–606PubMedGoogle Scholar
  43. Hanawa S (1993) An experimental study on the induction of anti-tumor immunological activity after cryosurgery for liver carcinoma, and the effect of concomitant immunotherapy with OK432. Nippon Geka Gakkai Zasshi 94:57–65PubMedGoogle Scholar
  44. Hänsler J, Neureiter D, Strobel D, Müller W, Mutter D, Bernatik T, Hahn EG, Becker D (2002) Cellular and vascular reactions in the liver to radiofrequency thermo-ablation with wet needle applicators. Study on juvenile domestic pigs. Eur Surg Res 34:357–363PubMedCrossRefGoogle Scholar
  45. Hänsler J, Wissniowski TT, Schuppan D, Witte A, Bernatik T, Hahn EG, Strobel D (2006) Activation and dramatically increased cytolytic activity of tumor specific T lymphocytes after radio-frequency ablation in patients with hepatocellular carcinoma and colorectal liver metastases. World J Gastroenterol 12:3716–3721PubMedCentralPubMedGoogle Scholar
  46. Heisterkamp J, van Hillegersberg R, Sinofsky E, Ijzermans JN (1997) Heat-resistant cylindrical diffuser for interstitial laser coagulation: comparison with the bare-tip fiber in a porcine liver model. Lasers Surg Med 20:304–309PubMedCrossRefGoogle Scholar
  47. Hill CR, ter Haar GR (1995) Review article: high intensity focused ultrasound – potential for cancer treatment. Br J Radiol 68:1296–1303PubMedCrossRefGoogle Scholar
  48. Hoffmann NE, Coad JE, Huot CS, Swanlund DJ, Bischof JC (2001) Investigation of the mechanism and the effect of cryoimmunology in the Copenhagen rat. Cryobiology 41:59–68CrossRefGoogle Scholar
  49. Hong K, Georgiades CS, Geschwind JF (2006) Technology insight: image-guided therapies for hepatocellular carcinoma—intra-arterial and ablative techniques. Nat Clin Pract Oncol 3:315–324PubMedCrossRefGoogle Scholar
  50. Hori K, Mihich E, Ehrke MJ (1989) Role of tumor necrosis factor and interleukin 1 in gamma-interferon-promoted activation of mouse tumoricidal macrophages. Cancer Res 49:2606–2614PubMedGoogle Scholar
  51. Hu Z, Yang XY, Liu Y, Morse MA, Lyerly HK, Clay TM, Zhong P (2005) Release of endogenous danger signals from HIFU-treated tumor cells and their stimulatory effects on APCs. Biochem Biophys Res Commun 335:124–131PubMedCentralPubMedCrossRefGoogle Scholar
  52. Hu Z, Yang XY, Liu Y, Sankin GN, Pua EC, Morse MA, Lyerly HK, Clay TM, Zhong P (2007) Investigation of HIFU-induced anti-tumor immunity in a murine tumor model. J Transl Med 5:34PubMedCentralPubMedCrossRefGoogle Scholar
  53. Hundt W, O’ Connell-Rodwell CE, Bednarski MD, Steinbach S, Guccione S (2007) In vitro effect of focused ultrasound or thermal stress on HSP70 expression and cell viability in three tumor cell lines. Acad Radiol 14:859–870PubMedCrossRefGoogle Scholar
  54. Isbert C, Ritz JP, Roggan A, Schuppan D, Ruhl M, Buhr HJ, Germer CT (2004) Enhancement of the immune response to residual intrahepatic tumor tissue by laser-induced thermotherapy (LITT) compared to hepatic resection. Lasers Surg Med 35:284–292PubMedCrossRefGoogle Scholar
  55. Ivarsson K, Myllymäki L, Jansner K, Bruun A, Stenram U, Tranberg KG (2003) Heat shock protein 70 (HSP70) after laser thermotherapy of an adenocarcinoma transplanted into rat liver. Anticancer Res 23:3703–3712PubMedGoogle Scholar
  56. Ivarsson K, Myllymäki L, Jansner K, Stenram U, Tranberg KG (2005) Resistance to tumor challenge after tumor laser thermotherapy is associated with a cellular immune response. Br J Cancer 93:435–440PubMedCentralPubMedCrossRefGoogle Scholar
  57. Joosten JJ, Muijen GH, Wobbes T, Ruers TJ (2001) In vivo destruction of tumor tissue by cryoablation can induce inhibition of secondary tumor growth: an experimental study. Cryobiology 41:49–58CrossRefGoogle Scholar
  58. Kallio R, Sequeiros R, Surcel HM, Ohtonen P, Kiviniemi H, Syrjälä H (2006) Early cytokine responses after percutaneous magnetic resonance imaging guided laser thermoablation of malignant liver tumors. Cytokine 34:278–283PubMedCrossRefGoogle Scholar
  59. Kennedy JE (2005) High-intensity focused ultrasound in the treatment of solid tumors. Nat Rev Cancer 5:321–327PubMedCrossRefGoogle Scholar
  60. Kirn A, Bingen A, Steffan AM, Wild MT, Keller F, Cinqualbre J (1982) Endocyticcapacities of Kupffer cells isolated from the human adult liver. Hepatology 2:216–222PubMedCrossRefGoogle Scholar
  61. Kramer G, Steiner GE, Grobl M, Hrachowitz K, Reithmayr F, Paucz L, Newman M, Madersbacher S, Gruber D, Susani M, Marberger M (2004) Response to sublethal heat treatment of prostatic tumor cells and of prostatic tumor infiltrating T-cells. Prostate 58:109–120PubMedCrossRefGoogle Scholar
  62. Kruse DE, Mackanos MA, O’Connell-Rodwell CE, Contag CH, Ferrara KW (2008) Short-duration-focused ultrasound stimulation of Hsp70 expression in vivo. Phys Med Biol 53:3641–3660PubMedCentralPubMedCrossRefGoogle Scholar
  63. Lau WY, Lai EC (2009) The current role of radiofrequency ablation in the management of hepatocellular carcinoma: a systematic review. Ann Surg 249:20–25PubMedCrossRefGoogle Scholar
  64. Liapi E, Geschwind JF (2007) Transcatheter and ablative therapeutic approaches for solid malignancies. J Clin Oncol 25:978–986PubMedCrossRefGoogle Scholar
  65. Lin JJ, Jin CN, Zheng ML, Ouyang XN, Zeng JX, Dai XH (2005) Clinical study on treatment of primary hepatocelluar carcinoma by Shenqi mixture combined with microwave coagulation. Chin J Integr Med 11:104–110PubMedCrossRefGoogle Scholar
  66. Liu K, Iyoda T, Saternus M, Kimura Y, Inaba K, Steinman RM (2002) Immune tolerance after delivery of dying cells to dendritic cells in situ. J Exp Med 196:1091–1097PubMedCentralPubMedCrossRefGoogle Scholar
  67. Liu F, Hu Z, Qiu L, Hui C, Li C, Zhong P, Zhang J (2010) Boosting high-intensity focused ultrasound-induced anti-tumor immunity using a sparse-scan strategy that can more effectively promote dendritic cell maturation. J Transl Med 8:7PubMedCentralPubMedCrossRefGoogle Scholar
  68. Lu P, Zhu XQ, Xu ZL, Zhou Q, Zhang J, Wu F (2009) Increased infiltration of activated tumor-infiltrating lymphocytes after high intensity focused ultrasound ablation of human breast cancer. Surgery 145:286–293PubMedCrossRefGoogle Scholar
  69. Lubbe AS, Bergemann C (1994) Ultrasound therapy for malignant tumors: a conceptual assessment. J Clin Ultrasound 22:113–117PubMedCrossRefGoogle Scholar
  70. Lutz MB, Schuler G (2002) Immature: semi-mature and fully mature dendritic cells: which signals induce tolerance or immunity? Trends Immunol 23:445–449PubMedCrossRefGoogle Scholar
  71. Machlenkin A, Goldberger O, Tirosh B, Paz A, Volovitz I, Bar-Haim E, Lee SH, Vadai E, Tzehoval E, Eisenbach L (2005) Combined dendritic cell cryotherapy of tumor induces systemic antimetastatic immunity. Clin Cancer Res 11:4955–4961PubMedCrossRefGoogle Scholar
  72. Madersbacher S, Gröbl M, Kramer G, Dirnhofer S, Steiner GE, Marberger M (1998) Regulation of heat shock protein 27 expression of prostatic cells in response to heat treatment. Prostate 37:174–181PubMedCrossRefGoogle Scholar
  73. Maris H, Balibar S (2000) Negative pressures and cavitation in liquid helium. Phys Today 53:29–32CrossRefGoogle Scholar
  74. Matsumoto R, Selig AM, Colucci VM, Jolesz FA (1992) Interstitial Nd:YAG laser ablation in normal rabbit liver: trial to maximize the size of laser-induced lesions. Lasers Surg Med 12:650–658PubMedCrossRefGoogle Scholar
  75. Matzinger P (2002) The danger model: a renewed sense of self. Science 296:301–305PubMedCrossRefGoogle Scholar
  76. Melief CJ (2008) Cancer immunotherapy by dendritic cells. Immunity 29:372–383PubMedCrossRefGoogle Scholar
  77. Meredith K, Haemmerich D, Qi C, Mahvi D (2007) Hepatic resection but not radiofrequency ablation results in tumor growth and increased growth factor expression. Ann Surg 245:771–776PubMedCentralPubMedCrossRefGoogle Scholar
  78. Miya K, Saji S, Morita T, Niwa H, Sakata K (1987) Experimental study on mechanism of absorption of cryonecrotized tumor antigens. Cryobiology 24:135–139PubMedCrossRefGoogle Scholar
  79. Möller PH, Ivarsson K, Stenram U, Radnell M, Tranberg KG (1998) Comparison between interstitial laser thermotherapy and excision of an adenocarcinoma transplanted into rat liver. Br J Cancer 77:1884–1892PubMedCrossRefGoogle Scholar
  80. Müller LC, Micksche M, Yamagata S, Kerschbaumer F (1985) Therapeutic effect of cryosurgery of murine osteosarcoma—influence on disease outcome and immune function. Cryobiology 22:77–85PubMedCrossRefGoogle Scholar
  81. Muralidharan V, Nikfarjam M, Malcontenti-Wilson C, Christophi C (2004) Effect of interstitial laser hyperthermia in a murine model of colorectal liver metastases: scanning electron microscopic study. World J Surg 28:33–37PubMedCrossRefGoogle Scholar
  82. Nakayama J, Kokuba H, Kobayashi J, Yoshida Y, Hori Y (1997a) Experimental approaches for the treatment of murine B16 melanomas of various sizes. I: local injection of ethanol with a combination of interleukin-2 or microwaval hyperthermia for B16 melanomas with a size of less than 7 mm in diameter. J Dermatol Sci 15:75–81PubMedCrossRefGoogle Scholar
  83. Nakayama J, Kokuba H, Kobayashi J, Yoshida Y, Hori Y (1997b) Experimental approaches for the treatment of murine B16 melanomas of various sizes. II: injection of ethanol with combinations of beta-interferon and microwaval hyperthermia for B16 melanomas with a size of greater than 10mm in diameter. J Dermatol Sci 15:82–88PubMedCrossRefGoogle Scholar
  84. Napoletano C, Taurino F, Biffoni M, De Majo A, Coscarella G, Bellati F, Rahimi H, Pauselli S, Pellicciotta I, Burchell JM, Gaspari LA, Ercoli L, Rossi P, Rughetti A (2008) RFA strongly modulates the immune system and anti-tumor immune responses in metastatic liver patients. Int J Oncol 32:481–490PubMedGoogle Scholar
  85. Nikfarjam M, Malcontenti-Wilson C, Christophi C (2005a) Focal hyperthermia produces progressive tumor necrosis independent of the initial thermal effects. J Gastrointest Surg 9:410–417PubMedCrossRefGoogle Scholar
  86. Nikfarjam M, Muralidharan V, Christophi C (2005b) Mechanisms of focal heat destruction of liver tumors. J Surg Res 127:208–223PubMedCrossRefGoogle Scholar
  87. Nikfarjam M, Muralidharan V, Su K, Malcontenti-Wilson C, Christophi C (2005c) Patterns of heat shock protein (HSP70) expression and Kupffer cell activity following thermal ablation of liver and colorectal liver metastases. Int J Hyperthermia 21:319–332PubMedCrossRefGoogle Scholar
  88. Ohno T, Kawano K, Sasaki A, Aramaki M, Yoshida T, Kitano S (2001) Expansion of an ablated site and induction of apoptosis after microwave coagulation therapy in rat liver. J Hepatobiliary Pancreat Surg 8:360–366PubMedCrossRefGoogle Scholar
  89. Osada S, Imai H, Tomita H, Tokuyama Y, Okumura N, Matsuhashi N, Sakashita F, Nonaka K (2007) Serum cytokine levels in response to hepatic cryoablation. J Surg Oncol 95:491–498PubMedCrossRefGoogle Scholar
  90. Overgaard J (1989) The current and potential role of hyperthermia in radiotherapy. Int J Radiat Oncol Biol Phys 16:537–549Google Scholar
  91. Ozaki T, Tabuse K, Tsuji T, Nakamura Y, Kakudo K, Mori I (2003a) Microwave cell death: enzyme histochemical evaluation for metastatic carcinoma of the liver. Pathol Int 53:837–845PubMedCrossRefGoogle Scholar
  92. Ozaki T, Mori I, Nakamura M, Utsunomiya H, Tabuse K, Kakudo K (2003b) Microwave cell death: immunohistochemical and enzyme histochemical evaluation. Pathol Int 53:686–692PubMedCrossRefGoogle Scholar
  93. Paulus JA, Tucker RD, Flanagan SW, Moseley PL, Loening SA, Park JB (1993) Heat shock protein response in a prostate tumor model to interstitial thermotherapy: implications for clinical treatment. Prostate 23:263–270PubMedCrossRefGoogle Scholar
  94. Peng Y, Martin DA, Kenkel J, Zhang K, Ogden CA, Elkon KB (2007) Innate and adaptive immune response to apoptotic cells. J Autoimmun 29:303–309PubMedCentralPubMedCrossRefGoogle Scholar
  95. Pockley AG (2003) Heat shock proteins as regulators of the immune response. Lancet 362:469–476PubMedCrossRefGoogle Scholar
  96. Rai R, Richardson C, Flecknell P, Robertson H, Burt A, Manas DM (2005) Study of apoptosis and heat shock protein (HSP) expression in hepatocytes following radiofrequency ablation (RFA). J Surg Res 129:147–151PubMedCrossRefGoogle Scholar
  97. Ravindranath MH, Wood TF, Soh D, Gonzales A, Muthugounder S, Perez C, Morton DL, Bilchik AJ (2002) Cryosurgical ablation of liver tumors in colon cancer patients increases the serum total ganglioside level and then selectively augments antiganglioside IgM. Cryobiology 45:10–21PubMedCrossRefGoogle Scholar
  98. Redondo P, del Olmo J, Lopez-Diaz de Cerio A, Inoges S, Marquina M, Melero I, Bendandi M (2007) Imiquimod enhances the systemic immunity attained by local cryosurgery destruction of melanoma lesions. J Invest Dermatol 127:1673–1680PubMedCrossRefGoogle Scholar
  99. Rock KL, Hearn A, Chen CJ, Shi Y (2006) Natural endogenous adjuvants. Springer Semin Immunopathol 26:231–246CrossRefGoogle Scholar
  100. Rosberger DF, Coleman DJ, Silverman R, Woods S, Rondeau M, Cunningham-Rundles S (1994) Immunomodulation in choroidal melanoma: reversal of inverted CD4+/CD8+ ratios following treatment with ultrasonic hyperthermia. Biotechnol Ther 5:59–68PubMedGoogle Scholar
  101. Rybak LD (2009) Fire and ice: thermal ablation of musculoskeletal tumors. Radiol Clin North Am 47:455–469PubMedCrossRefGoogle Scholar
  102. Rylander MN, Feng Y, Zhang Y, Bass J, Stafford RJ, Volgin A, Hazle JD, Diller KR (2006) Optimizing heat shock protein expression induced by prostate cancer laser therapy through predictive computational models. J Biomed Opt 11:041113PubMedCrossRefGoogle Scholar
  103. Sabel MS (2009) Cryo-immunology: a review of the literature and proposed mechanisms for stimulatory versus suppressive immune responses. Cryobiology 58:1–11PubMedCrossRefGoogle Scholar
  104. Sabel MS, Nehs MA, Su G, Lowler KP, Ferrara JL, Chang AE (2005) Immunologic response to cryoablation of breast cancer. Breast Cancer Res Treat 90:97–104PubMedCrossRefGoogle Scholar
  105. Sabharwal T, Katsanos K, Buy X, Gangi A (2009) Image-guided ablation therapy of bone tumors. Semin Ultrasound CT MR 30:78–90PubMedCrossRefGoogle Scholar
  106. Sadamori H, Yagi T, Kanaoka Y, Morimoto Y, Inagaki M, Ishikawa T, Matsukawa H, Matsuda H, Iwagaki H, Tanaka N (2003) The analysis of the usefulness of laparoscopic microwave coagulation therapy for hepatocellular carcinoma in patients with poor hepatic reserve by serial measurements of IL-6, cytokine antagonists, and C-reactive protein. Surg Endosc 17:510–514PubMedCrossRefGoogle Scholar
  107. Sadikot RT, Wudel LJ, Jansen DE, Debelak JP, Yull FE, Christman JW, Blackwell TS, Chapman WC (2002) Hepatic cryoablation-induced multisystem injury: bioluminescent detection of NF-kappaB activation in a transgenic mouse model. J Gastrointest Surg 6:264–270PubMedCrossRefGoogle Scholar
  108. Saito K, Haas A, Albelda S, Li D, O’Malley BW (2005) Combination of immunotherapy with radiofrequency ablation for head and neck cancer. Otolaryngol Head Neck Surg 133:98–99CrossRefGoogle Scholar
  109. Saji H, Song W, Nakamura H, Saijo T, Hosaka M, Hagiwara M, Ogata A, Kawasaki N, Engleman EG, Kato H (2006) A possibility of overcoming local tumor immune tolerance by radiofrequency ablation in combination with intratumoral injection of naïve dendritic cell. Gan To Kagaku Ryoho 33:1736–1738PubMedGoogle Scholar
  110. Sauter B, Albert ML, Francisco L, Larsson M, Somersan S, Bhardwaj N (2000) 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 191:423–434PubMedCentralPubMedCrossRefGoogle Scholar
  111. Savill J, Dransfield I, Gregory C, Haslett C (2002) A blast from the past: clearance of apoptotic cells regulates immune responses. Nat Rev Immunol 2:965–975PubMedCrossRefGoogle Scholar
  112. Scheffer SR, Nave H, Korangy F, Schlote K, Pabst R, Jaffee EM, Manns MP, Greten TF (2003) Apoptotic, but not necrotic, tumor cell vaccines induce a potent immune response in vivo. Int J Cancer 103:205–211PubMedCrossRefGoogle Scholar
  113. Schell SR, Wessels FJ, Abouhamze A, Moldawer LL, Copeland EM (2002) Pro- and antiinflammatory cytokine production after radiofrequency ablation of unresectable hepatic tumors. J Am Coll Surg 195:774–781PubMedCrossRefGoogle Scholar
  114. Schnurr M, Scholz C, Rothenfusser S, Galambos P, Dauer M, Röbe H, Endres S, Eigler A (2002) Apoptotic pancreatic tumor cells are superior to cell lysates in promoting cross-priming of cytotoxic T-cells and activate NK and gammadelta T cells. Cancer Res 62:2347–2352PubMedGoogle Scholar
  115. Schueller G, Stift A, Friedl J, Dubsky P, Bachleitner-Hofmann T, Benkoe T, Jakesz R, Gnant M (2003) Hyperthermia improves cellular immune response to human hepatocellular carcinoma subsequent to co-culture with tumor lysate pulsed dendritic cells. Int J Oncol 22:1397–1402PubMedGoogle Scholar
  116. Schueller G, Kettenbach J, Sedivy R, Bergmeister H, Stift A, Fried J, Gnant M, Lammer J (2004) Expression of heat shock proteins in human hepatocellular carcinoma after radiofrequency ablation in an animal model. Oncol Rep 12:495–499PubMedGoogle Scholar
  117. Seifert JK, Junginger T (2004) Cryotherapy for liver tumors: current status, perspectives, clinical results, and review of literature. Technol Cancer Res Treat 3:151–163PubMedCrossRefGoogle Scholar
  118. Seifert JK, France MP, Zhao J, Bolton EJ, Finlay I, Junginger T, Morris DL (2002) 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 26:1333–1341PubMedCrossRefGoogle Scholar
  119. Shibata T, Yamashita T, Suzuki K, Takeichi N, Micallef M, Hosokawa M, Kobayashi H, Murata M, Arisue M (1998) Enhancement of experimental pulmonary metastasis and inhibition of subcutaneously transplanted tumor growth following cryosurgery. Anticancer Res 18:4443–4448PubMedGoogle Scholar
  120. Si T, Guo Z, Hao X (2008) Immunologic response to primary cryoablation of high-risk prostate cancer. Cryobiology 57:66–71PubMedCrossRefGoogle Scholar
  121. Si T, Guo Z, Hao X (2009) Combined cryoablation and GM-CSF treatment for metastatic hormone refractory prostate cancer. J Immunother 32:86–91PubMedCrossRefGoogle Scholar
  122. Simon CJ, Dupuy DE, Mayo-Smith WW (2005) Microwave ablation: principles and applications. Radiographics 25:S69–S83PubMedCrossRefGoogle Scholar
  123. Skoberne M, Beignon AS, Bhardwaj N (2004) Danger signals: a time and space continuum. Trends Mol Med 10:251–257PubMedCrossRefGoogle Scholar
  124. Szmigielski S, Sobczynski J, Sokolska G, Stawarz B, Zielinski H, Petrovich Z (1991) Effects of local prostatic hyperthermia on human NK and T cell function. Int J Hyperthermia 7:869–880PubMedCrossRefGoogle Scholar
  125. ter Haar G (2007) Therapeutic applications of ultrasound. Prog Biophys Mol Biol 93:111–129PubMedCrossRefGoogle Scholar
  126. Thomsen S (1991) Pathologic analysis of photothermal and photomechanical effects of laser-tissue interactions. Photochem Photobiol 53:825–835PubMedCrossRefGoogle Scholar
  127. Timmerman RD, Bizekis CS, Pass HI, Fong Y, Dupuy DE, Dawson LA, Lu D (2009) Local surgical, ablative, and radiation treatment of metastases. CA Cancer J Clin 59:145–170PubMedCrossRefGoogle Scholar
  128. Todryk SM, Michael J, Goughy MJ, Pockley AG (2003) Facets of heat shock protein 70 show immunotherapeutic potential. Immunology 110:1–9PubMedCentralPubMedCrossRefGoogle Scholar
  129. Tranberg KG (2004) Percutaneous ablation of liver tumors. Best Pract Res Clin Gastroenterol 18:125–145PubMedCrossRefGoogle Scholar
  130. Udagawa M, Kudo-Saito C, Hasegawa G, Yano K, Yamamoto A, Yaguchi M, Toda M, Azuma I, Iwai T, Kawakami K (2006) Enhancement of immunologic tumor regression by intratumoral administration of dendritic cells in combination with cryoablative tumor pretreatment and bacillus calmetteguerin cell wall skeleton stimulation. Clin Cancer Res 12:7465–7475PubMedCrossRefGoogle Scholar
  131. Urano M, Tanaka C, Sugiyama Y, Miya K, Saji S (2003) Antitumor effects of residual tumor after cryoablation: the combined effect of residual tumor and a protein-bound polysaccharaide on multiple liver metastases in a murine model. Cryobiology 46:238–245PubMedCrossRefGoogle Scholar
  132. van Duijnhoven FH, Tollenaar RA, Terpstra OT, Kuppen PJ (2005) Locoregional therapies of liver metastases in a rat CC531 coloncarcinoma model results in increased resistance to tumor rechallenge. Clin Exp Metastasis 22:247–253PubMedCrossRefGoogle Scholar
  133. Viorritto ICB, Nikolov NP, Siegel RM (2007) Autoimmunity versus tolerance: can dying cells tip the balance? Clin Immunol 122:125–134PubMedCrossRefGoogle Scholar
  134. Vogl TJ, Wissniowski TT, Naguib NN, Hammerstingl RM, Mack MG, Münch S, Ocker M, Strobel D, Hahn EG, Hänsler J (2009) Activation of tumor-specific T lymphocytes after laser-induced thermotherapy in patients with colorectal liver metastases. Cancer Immunol Immunother 58:1557–1563PubMedCrossRefGoogle Scholar
  135. Wang X, Sun J (2002) High-intensity focused ultrasound in patients with late-stage pancreatic carcinoma. Chin Med J 115:1332–1335PubMedGoogle Scholar
  136. Washington K, Debelak JP, Gobbell C, Sztipanovits DR, Shyr Y, Olson S, Chapman WC (2001) Hepatic cryoablation-induced acute lung injury: histopathologic findings. J Surg Res 95:1–7PubMedCrossRefGoogle Scholar
  137. Watanabe N, Niitsu Y, Umeno H, Kuriyama H, Neda H, Yamauchi N, Maeda M, Urushizaki I (1988) Toxic effect of tumor necrosis factor on tumor vasculature in mice. Cancer Res 48:2179–2183PubMedGoogle Scholar
  138. Wheatley DN, Kerr C, Gregory DW (1989) Heat-induced damage to HeLa-S3 cells: correlation of viability, permeability, osmosensitivity, phase-contrast light-, scanning electron- and transmission electron-microscopical findings. Int J Hyperthermia 5:145–162PubMedCrossRefGoogle Scholar
  139. Wiersinga WJ, Jansen MC, Straatsburg IH, Davids PH, Klaase JM, Gouma DJ, van Gulik TM (2003) Lesion progression with time and the effect of vascular occlusion following radiofrequency ablation of the liver. Br J Surg 90:306–312PubMedCrossRefGoogle Scholar
  140. Wissniowski TT, Hänsler J, Neureiter D, Frieser M, Schaber S, Esslinger B, Voll R, Strobel D, Hahn EG, Schuppan D (2003) Activation of tumorspecific T lymphocytes by radio-frequency ablation of the VX2 hepatoma in rabbits. Cancer Res 63:6496–6500PubMedGoogle Scholar
  141. Wu F (2006) Extracorporeal high intensity focused ultrasound in the treatment of patients with solid malignancy. Minim Invasive Ther Allied Technol 15:26–35PubMedCrossRefGoogle Scholar
  142. Wu F, Wang ZB, Lu P, Xu ZL, Chen WZ, Zhu H, Jin CB (2004) Activated anti-tumor immunity in cancer patients after high intensity focused ultrasound ablation. Ultrasound Med Biol 30:1217–1222PubMedCrossRefGoogle Scholar
  143. Wu F, Zhou L, Chen WR (2007a) Host antitumour immune responses to HIFU ablation. Int J Hyperthermia 23:165–171PubMedCrossRefGoogle Scholar
  144. Wu F, Wang ZB, Cao YD, Zhou Q, Zhang J, Xu ZL, Zhu XQ (2007b) Expression of tumor antigens and heat-shock protein 70 in breast cancer cells after high-intensity focused ultrasound ablation. Ann Surg Oncol 14:1237–1242PubMedCrossRefGoogle Scholar
  145. Wudel LJ, Allos TM, Washington MK, Sheller JR, Chapman WC (2003) Multi-organ inflammation after hepatic cryoablation in BALB/c mice. J Surg Res 112:131–137PubMedCrossRefGoogle Scholar
  146. Xia JZ, Xie FL, Ran LF, Xie XP, Fan YM, Wu F (2012) High-intensity focused ultrasound tumor ablation activates autologous tumor-specific cytotoxic T lymphocytes. Ultrasound Med Biol 38:1363–1371PubMedCrossRefGoogle Scholar
  147. Xing Y, Lu X, Pua EC, Zhong P (2008) The effect of high intensity focused ultrasound treatment on metastases in a murine melanoma model. Biochem Biophys Res Commun 375:645–650PubMedCentralPubMedCrossRefGoogle Scholar
  148. Xu ZL, Zhu XQ, Lu P, Zhou Q, Zhang J, Wu F (2009) Activation of tumor-infiltrating antigen presenting cells by high intensity focused ultrasound ablation of human breast cancer. Ultrasound Med Biol 35:50–57PubMedCrossRefGoogle Scholar
  149. Yang R, Reilly CR, Rescorla FJ, Sanghvi NT, Fry FJ, Franklin TD, Grosfeld JL (1992) Effects of high-intensity focused ultrasound in the treatment of experimental neuroblastoma. J Pediatr Surg 27:246–250PubMedCrossRefGoogle Scholar
  150. Yao LC, Yang RL (2007) Immunotherapy against tumor with dendritic cell sensitized by necrotic tumor tissue after microwave coagulation therapy. Zhonghua Yi Xue Za Zhi 87:2552–2556PubMedGoogle Scholar
  151. Zerbini A, Pilli M, Penna A, Pelosi G, Schianchi C, Molinari A, Schivazappa S, Zibera C, Fagnoni FF, Ferrari C, Missale G (2006) Radiofrequency thermal ablation of hepatocellular carcinoma liver nodules can activate and enhance tumor-specific T-cell responses. Cancer Res 66:1139–1146PubMedCrossRefGoogle Scholar
  152. Zerbini A, Pilli M, Fagnoni F, Pelosi G, Pizzi MG, Schivazappa S, Laccabue D, Cavallo C, Schianchi C, Ferrari C, Missale G (2008) Increased immunostimulatory activity conferred to antigen-presenting cells by exposure to antigen extract from hepatocellular carcinoma after radiofrequency thermal ablation. J Immunother 31:271–282PubMedCrossRefGoogle Scholar
  153. Zhang J, Dong B, Liang P, Yu X, Su L, Yu D, Ji X, Yu G (2002) Significance of changes in local immunity in patients with hepatocellular carcinoma after percutaneous microwave coagulation therapy. Chin Med J 115:1367–1371PubMedGoogle Scholar
  154. Zhang JP, Pan HM, Huang LP, Huang LP, Wu JM (2006) Impact of radiofrequency on splenocyte immunity of mice bearing H22 liver cancer. Ai Zheng 25:34–39PubMedGoogle Scholar
  155. Zhang Y, Deng J, Feng J, Wu F (2010) Enhancement of antitumor vaccine in ablated hepatocellular carcinoma by high-intensity focused ultrasound: a preliminary report. World J Gastroenterol 16:3584–3591PubMedCentralPubMedCrossRefGoogle Scholar
  156. Zhou P, Fu M, Bai J, Wang Z, Wu F (2007) Immune response after high-intensity focused ultrasound ablation for H22 tumor. J Clin Oncol 25:21169Google Scholar
  157. Zhou Q, Zhu XQ, Zhang J, Xu ZL, Lu P, Wu F (2008) Changes in circulating immunosuppressive cytokine levels of cancer patients after high intensity focused ultrasound treatment. Ultrasound Med Biol 34:81–88PubMedCrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  1. 1.Nuffield Department of Surgical SciencesHIFU Unit, Churchill Hospital, University of OxfordOxfordUK
  2. 2.Institute of Ultrasonic Engineering in MedicineCollege of Biomedical Engineering, Chongqing Medical UniversityChongqingChina

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