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Gastroenterology Research and Practice
Volume 2016, Article ID 9251375, 11 pages
http://dx.doi.org/10.1155/2016/9251375
Review Article

Thermal Ablative Therapies and Immune Checkpoint Modulation: Can Locoregional Approaches Effect a Systemic Response?

1University of Pittsburgh, Pittsburgh, PA 15213, USA
2Mayo Clinic, Scottsdale, AZ 85259, USA
3MD Anderson Cancer Center, Houston, TX 77030, USA

Received 20 December 2015; Accepted 16 February 2016

Academic Editor: Nicola Silvestris

Copyright © 2016 Amol Mehta et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. A. Wells, J. L. Hinshaw, M. G. Lubner, T. J. Ziemlewicz, C. L. Brace, and F. T. Lee, “Liver ablation: best practice,” Radiologic Clinics of North America, vol. 53, pp. 933–971, 2015. View at Google Scholar
  2. K. F. Chu and D. E. Dupuy, “Thermal ablation of tumours: biological mechanisms and advances in therapy,” Nature Reviews Cancer, vol. 14, no. 3, pp. 199–208, 2014. View at Publisher · View at Google Scholar · View at Scopus
  3. N. Rozenblum, E. Zeira, V. Scaiewicz et al., “Oncogenesis: an ‘off-target’ effect of radiofrequency ablation,” Radiology, vol. 276, no. 2, pp. 426–432, 2015. View at Publisher · View at Google Scholar
  4. M. Nikfarjam, V. Muralidharan, and C. Christophi, “Mechanisms of focal heat destruction of liver tumors,” Journal of Surgical Research, vol. 127, no. 2, pp. 208–223, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. Y. Keisari, Tumor Ablation, Springer Science & Business Media, Dordrecht, The Netherlands, 2012. View at Publisher · View at Google Scholar
  6. C. W. Song, H. Park, and R. J. Griffin, “Improvement of tumor oxygenation by mild hyperthermia,” Radiation Research, vol. 155, no. 4, pp. 515–528, 2001. View at Publisher · View at Google Scholar · View at Scopus
  7. E. L. Jones, M.-J. Zhao, M. A. Stevenson, and S. K. Calderwood, “The 70 kilodalton heat shock protein is an inhibitor of apoptosis in prostate cancer,” International Journal of Hyperthermia, vol. 20, no. 8, pp. 835–849, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. D. Tang, M. A. Khaleque, E. L. Jones et al., “Expression of heat shock proteins and heat shock protein messenger ribonucleic acid in human prostate carcinoma in vitro and in tumors in vivo,” Cell Stress and Chaperones, vol. 10, no. 1, pp. 46–58, 2005. View at Publisher · View at Google Scholar · View at Scopus
  9. M. H. M. G. M. den Brok, R. P. M. Sutmuller, S. Nierkens et al., “Efficient loading of dendritic cells following cryo and radiofrequency ablation in combination with immune modulation induces anti-tumour immunity,” British Journal of Cancer, vol. 95, no. 7, pp. 896–905, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Ghanamah, E. Berber, and A. Siperstein, “Pattern of carcinoembryonic antigen drop after laparoscopic radiofrequency ablation of liver metastasis from colorectal carcinoma,” Cancer, vol. 107, no. 1, pp. 149–153, 2006. View at Publisher · View at Google Scholar
  11. T. Ohno, K. Kawano, A. Sasaki, M. Aramaki, T. Yoshida, and S. Kitano, “Expansion of an ablated site and induction of apoptosis after microwave coagulation therapy in rat liver,” Journal of Hepato-Biliary-Pancreatic Surgery, vol. 8, no. 4, pp. 360–366, 2001. View at Publisher · View at Google Scholar · View at Scopus
  12. L. Zitvogel, N. Casares, M. O. Péquignot, N. Chaput, M. L. Albert, and G. Kroemer, “Immune response against dying tumor cells,” Advances in Immunology, vol. 84, pp. 131–179, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. D. S. K. Lu, S. S. Raman, D. J. Vodopich, M. Wang, J. Sayre, and C. Lassman, “Effect of vessel size on creation of hepatic radiofrequency lesions in pigs: assessment of the ‘heat sink’ effect,” American Journal of Roentgenology, vol. 178, no. 1, pp. 47–51, 2002. View at Publisher · View at Google Scholar · View at Scopus
  14. D. S. K. Lu, S. S. Raman, P. Limanond et al., “Influence of large peritumoral vessels on outcome of radiofrequency ablation of liver tumors,” Journal of Vascular and Interventional Radiology, vol. 14, no. 10, pp. 1267–1274, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. S. M. Thompson, M. R. Callstrom, K. A. Butters et al., “Heat stress induced cell death mechanisms in hepatocytes and hepatocellular carcinoma: in vitro and in vivo study,” Lasers in Surgery and Medicine, vol. 46, no. 4, pp. 290–301, 2014. View at Publisher · View at Google Scholar · View at Scopus
  16. R. L. Warters and J. L. Roti Roti, “Hyperthermia and the cell nucleus,” Radiation Research, vol. 92, no. 3, pp. 458–462, 1982. View at Publisher · View at Google Scholar · View at Scopus
  17. L.-S. Teng, K.-T. Jin, N. Han, and J. Cao, “Radiofrequency ablation, heat shock protein 70 and potential anti-tumor immunity in hepatic and pancreatic cancers: a minireview,” Hepatobiliary and Pancreatic Diseases International, vol. 9, no. 4, pp. 361–365, 2010. View at Google Scholar · View at Scopus
  18. S. N. Goldberg, M. Ahmed, G. S. Gazelle et al., “Radio-frequency thermal ablation with NaCl solution injection: effect of electrical conductivity on tissue heating and coagulation-phantom and porcine liver study,” Radiology, vol. 219, no. 1, pp. 157–165, 2001. View at Publisher · View at Google Scholar · View at Scopus
  19. L. Zhang, N. Wang, Q. Shen, W. Cheng, and G.-J. Qian, “Therapeutic efficacy of percutaneous radiofrequency ablation versus microwave ablation for hepatocellular carcinoma,” PLoS ONE, vol. 8, no. 10, Article ID e76119, 2013. View at Publisher · View at Google Scholar
  20. M. G. Lubner, C. L. Brace, J. L. Hinshaw, and F. T. Lee Jr., “Microwave tumor ablation: mechanism of action, clinical results, and devices,” Journal of Vascular and Interventional Radiology, vol. 21, no. 8, pp. S192–S203, 2010. View at Publisher · View at Google Scholar · View at Scopus
  21. J. P. Erinjeri and T. W. I. Clark, “Cryoablation: mechanism of action and devices,” Journal of Vascular and Interventional Radiology, vol. 21, no. 8, pp. S187–S191, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. J. G. Baust and A. A. Gage, “The molecular basis of cryosurgery,” BJU International, vol. 95, no. 9, pp. 1187–1191, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. A. A. Gage and J. Baust, “Mechanisms of tissue injury in cryosurgery,” Cryobiology, vol. 37, no. 3, pp. 171–186, 1998. View at Publisher · View at Google Scholar · View at Scopus
  24. C. Bastianpillai, N. Petrides, T. Shah, S. Guillaumier, H. U. Ahmed, and M. Arya, “Harnessing the immunomodulatory effect of thermal and non-thermal ablative therapies for cancer treatment,” Tumor Biology, vol. 36, no. 12, pp. 9137–9146, 2015. View at Publisher · View at Google Scholar
  25. P. Sharma and J. P. Allison, “The future of immune checkpoint therapy,” Science, vol. 348, no. 6230, pp. 56–61, 2015. View at Publisher · View at Google Scholar
  26. T. Pradeu and E. L. Cooper, “The danger theory: 20 years later,” Frontiers in Immunology, vol. 3, article 287, 2012. View at Publisher · View at Google Scholar · View at Scopus
  27. T. A. Ferguson, J. Choi, and D. R. Green, “Armed response: how dying cells influence T-cell functions,” Immunological Reviews, vol. 241, no. 1, pp. 77–88, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. C. Yantorno, W. A. Soanes, M. J. Gonder, and S. Shulman, “Studies in cryo-immunology. I. The production of antibodies to urogenital tissue in consequence of freezing treatment,” Immunology, vol. 12, no. 4, pp. 395–410, 1967. View at Google Scholar · View at Scopus
  29. F. Wu, L. Zhou, and W. R. Chen, “Host antitumour immune responses to HIFU ablation,” International Journal of Hyperthermia, vol. 23, no. 2, pp. 165–171, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. F. Wu, Z.-B. Wang, Y.-D. Cao et al., “‘Wide local ablation’ of localized breast cancer using high intensity focused ultrasound,” Journal of Surgical Oncology, vol. 96, pp. 130–136, 2007. View at Google Scholar
  31. M. Y. Ali, C. F. Grimm, M. Ritter et al., “Activation of dendritic cells by local ablation of hepatocellular carcinoma,” Journal of Hepatology, vol. 43, no. 5, pp. 817–822, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. A. M. Fietta, M. Morosini, I. Passadore et al., “Systemic inflammatory response and downmodulation of peripheral CD25+Foxp3+ T-regulatory cells in patients undergoing radiofrequency thermal ablation for lung cancer,” Human Immunology, vol. 70, no. 7, pp. 477–486, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. J. P. Erinjeri, C. T. Thomas, A. Samoilia et al., “Image-guided thermal ablation of tumors increases the plasma level of interleukin-6 and interleukin-10,” Journal of Vascular and Interventional Radiology, vol. 24, no. 8, pp. 1105–1112, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. F. Ahmad, G. Gravante, N. Bhardwaj et al., “Changes in interleukin-1β and 6 after hepatic microwave tissue ablation compared with radiofrequency, cryotherapy and surgical resections,” American Journal of Surgery, vol. 200, no. 4, pp. 500–506, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. T. Chen, J. Guo, C. Han, M. Yang, and X. Cao, “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,” Journal of Immunology, vol. 182, no. 3, pp. 1449–1459, 2009. View at Publisher · View at Google Scholar · View at Scopus
  36. E. Schmitt, M. Gehrmann, M. Brunet, G. Multhoff, and C. Garrido, “Intracellular and extracellular functions of heat shock proteins: repercussions in cancer therapy,” Journal of Leukocyte Biology, vol. 81, no. 1, pp. 15–27, 2007. View at Publisher · View at Google Scholar · View at Scopus
  37. S. A. Dromi, M. P. Walsh, S. Herby et al., “Radiofrequency ablation induces antigen-presenting cell infiltration and amplification of weak tumor-induced immunity,” Radiology, vol. 251, no. 1, pp. 58–66, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. C. Figueiredo, M. Wittmann, D. Wang et al., “Heat shock protein 70 (HSP70) induces cytotoxicity of T-helper cells,” Blood, vol. 113, no. 13, pp. 3008–3016, 2009. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Tesniere, T. Panaretakis, O. Kepp et al., “Molecular characteristics of immunogenic cancer cell death,” Cell Death and Differentiation, vol. 15, no. 1, pp. 3–12, 2008. View at Publisher · View at Google Scholar · View at Scopus
  40. G. Multhoff, A. G. Pockley, C. Streffer, and U. S. Gaipl, “Dual role of heat shock proteins (HSPs) in anti-tumor immunity,” Current Molecular Medicine, vol. 12, no. 9, pp. 1174–1182, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. S. P. Haen, C. Gouttefangeas, D. Schmidt et al., “Elevated serum levels of heat shock protein 70 can be detected after radiofrequency ablation,” Cell Stress and Chaperones, vol. 16, no. 5, pp. 495–504, 2011. View at Publisher · View at Google Scholar · View at Scopus
  42. T. Kottke, L. Sanchez-Perez, R. M. Diaz et al., “Induction of hsp70-mediated Th17 autoimmunity can be exploited as immunotherapy for metastatic prostate cancer,” Cancer Research, vol. 67, no. 24, pp. 11970–11979, 2007. View at Publisher · View at Google Scholar · View at Scopus
  43. K. Hiroishi, J. Eguchi, T. Baba et al., “Strong CD8+ T-cell responses against tumor-associated antigens prolong the recurrence-free interval after tumor treatment in patients with hepatocellular carcinoma,” Journal of Gastroenterology, vol. 45, no. 4, pp. 451–458, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. T. T. Wissniowski, J. Hünsler, D. Neureiter et al., “Activation of tumor-specific T lymphocytes by radio-frequency ablation of the VX2 hepatoma in rabbits,” Cancer Research, vol. 63, no. 19, pp. 6496–6500, 2003. View at Google Scholar · View at Scopus
  45. E. Unitt, A. Marshall, W. Gelson et al., “Tumour lymphocytic infiltrate and recurrence of hepatocellular carcinoma following liver transplantation,” Journal of Hepatology, vol. 45, no. 2, pp. 246–253, 2006. View at Publisher · View at Google Scholar · View at Scopus
  46. M. Widenmeyer, Y. Shebzukhov, S. P. Haen et al., “Analysis of tumor antigen-specific T cells and antibodies in cancer patients treated with radiofrequency ablation,” International Journal of Cancer, vol. 128, no. 11, pp. 2653–2662, 2011. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Ahmed, G. Kumar, M. Moussa et al., “Hepatic radiofrequency ablation-induced stimulation of distant tumor growth is suppressed by c-Met inhibition,” Radiology, 2015. View at Publisher · View at Google Scholar
  48. R. Lencioni, D. Cioni, L. Crocetti et al., “Early-stage hepatocellular carcinoma in patients with cirrhosis: long-term results of percutaneous image-guided radiofrequency ablation,” Radiology, vol. 234, no. 3, pp. 961–967, 2005. View at Publisher · View at Google Scholar · View at Scopus
  49. M. W. Nijkamp, J. D. W. van der Bilt, M. T. de Bruijn et al., “Accelerated perinecrotic outgrowth of colorectal liver metastases following radiofrequency ablation is a hypoxia-driven phenomenon,” Annals of Surgery, vol. 249, no. 5, pp. 814–823, 2009. View at Publisher · View at Google Scholar · View at Scopus
  50. M. W. Nijkamp, A. Borren, K. M. Govaert et al., “Radiofrequency ablation of colorectal liver metastases induces an inflammatory response in distant hepatic metastases but not in local accelerated outgrowth,” Journal of Surgical Oncology, vol. 101, no. 7, pp. 551–556, 2010. View at Publisher · View at Google Scholar · View at Scopus
  51. J. Kong, J. Kong, B. Pan et al., “Insufficient radiofrequency ablation promotes angiogenesis of residual hepatocellular carcinoma via HIF-1α/VEGFA,” PloS ONE, vol. 7, no. 5, Article ID e37266, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. S. A. Solazzo, M. Ahmed, R. Schor-Bardach et al., “Liposomal doxorubicin increases radiofrequency ablation-induced tumor destruction by increasing cellular oxidative and nitrative stress and accelerating apoptotic pathways,” Radiology, vol. 255, no. 1, pp. 62–74, 2010. View at Publisher · View at Google Scholar · View at Scopus
  53. W. Yang, M. Ahmed, B. Tasawwar et al., “Radiofrequency ablation combined with liposomal quercetin to increase tumour destruction by modulation of heat shock protein production in a small animal model,” International Journal of Hyperthermia, vol. 27, no. 6, pp. 527–538, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Ahmed, G. Kumar, G. Navarro et al., “Systemic siRNA nanoparticle-based drugs combined with radiofrequency ablation for cancer therapy,” PLoS ONE, vol. 10, no. 7, Article ID e0128910, 2015. View at Publisher · View at Google Scholar
  55. R. J. Ablin, W. A. Soanes, and M. J. Gonder, “Prospects for cryo-immunotherapy in cases of metastasizing carcinoma of the prostate,” Cryobiology, vol. 8, no. 3, pp. 271–279, 1971. View at Publisher · View at Google Scholar · View at Scopus
  56. E. Gursel, M. Roberts, and R. J. Veenema, “Regression of prostatic cancer following sequential cryotherapy to the prostate,” Journal of Urology, vol. 108, no. 6, pp. 928–932, 1972. View at Google Scholar · View at Scopus
  57. C. E. Blackwood and I. S. Cooper, “Response of experimental tumor systems to cryosurgery,” Cryobiology, vol. 9, no. 6, pp. 508–515, 1972. View at Publisher · View at Google Scholar · View at Scopus
  58. W. A. Soanes, R. J. Ablin, and M. J. Gonder, “Remission of metastatic lesions following cryosurgery in prostatic cancer: immunologic considerations,” Journal of Urology, vol. 104, no. 1, pp. 154–159, 1970. View at Google Scholar · View at Scopus
  59. S. Tanaka, “Immunological aspects of cryosurgery in general surgery,” Cryobiology, vol. 19, no. 3, pp. 247–262, 1982. View at Publisher · View at Google Scholar · View at Scopus
  60. H. B. Neel, A. S. Ketcham, and W. G. Hammond, “Experimental evaluation of in situ oncocide for primary tumor therapy: comparison of tumor-specific immunity after complete excision, cryonecrosis and ligation,” Laryngoscope, vol. 83, no. 3, pp. 376–387, 1973. View at Publisher · View at Google Scholar · View at Scopus
  61. M. S. Sabel, M. A. Nehs, G. Su, K. P. Lowler, J. L. M. Ferrara, and A. E. Chang, “Immunologic response to cryoablation of breast cancer,” Breast Cancer Research and Treatment, vol. 90, no. 1, pp. 97–104, 2005. View at Publisher · View at Google Scholar · View at Scopus
  62. M. C. Jansen, R. van Hillegersberg, I. G. Schoots et al., “Cryoablation induces greater inflammatory and coagulative responses than radiofrequency ablation or laser induced thermotherapy in a rat liver model,” Surgery, vol. 147, no. 5, pp. 686–695, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. W. C. Chapman, J. P. Debelak, C. W. Pinson et al., “Hepatic cryoablation, but not radiofrequency ablation, results in lung inflammation,” Annals of Surgery, vol. 231, no. 5, pp. 752–761, 2000. View at Publisher · View at Google Scholar · View at Scopus
  64. T. Yamashita, K. Hayakawa, M. Hosokawa et al., “Enhanced tumor metastases in rats following cryosurgery of primary tumor,” Gan, vol. 73, no. 2, pp. 222–228, 1982. View at Google Scholar · View at Scopus
  65. T. Shibata, T. Yamashita, K. Suzuki et al., “Enhancement of experimental pulmonary metastasis and inhibition of subcutaneously transplanted tumor growth following cryosurgery,” Anticancer Research, vol. 18, no. 6 A, pp. 4443–4448, 1998. View at Google Scholar · View at Scopus
  66. T. Shibata, K. Suzuki, T. Yamashita et al., “Immunological analysis of enhanced spontaneous metastasis in WKA rats following cryosurgery,” Anticancer Research, vol. 18, no. 4, pp. 2483–2486, 1998. View at Google Scholar · View at Scopus
  67. K. Hayakawa, T. Yamashita, K. Suzuki et al., “Comparative immunological studies in rats following cryosurgery and surgical excision of 3-methylcholanthrene-induced primary autochthonous tumors,” Gan, vol. 73, no. 3, pp. 462–469, 1982. View at Google Scholar · View at Scopus
  68. M. S. Sabel, G. Su, K. A. Griffith, and A. E. Chang, “Rate of freeze alters the immunologic response after cryoablation of breast cancer,” Annals of Surgical Oncology, vol. 17, no. 4, pp. 1187–1193, 2010. View at Publisher · View at Google Scholar · View at Scopus
  69. M. G. Wing, K. Rogers, G. Jacob, and R. C. Rees, “Characterisation of suppressor cells generated following cryosurgery of an HSV-2-induced fibrosarcoma,” Cancer Immunology Immunotherapy, vol. 26, no. 2, pp. 169–175, 1988. View at Google Scholar · View at Scopus
  70. S. Hanawa, “An experimental study on the induction of anti-tumor immunological activity after cryosurgery for liver carcinoma, and the effect of concomitant immunotherapy with OK432,” Nihon Geka Gakkai Zasshi, vol. 94, no. 1, pp. 57–65, 1993. View at Google Scholar · View at Scopus
  71. M. Urano, C. Tanaka, Y. Sugiyama, K. Miya, and S. Saji, “Antitumor effects of residual tumor after cryoablation: The combined effect of residual tumor and a protein-bound polysaccharide on multiple liver metastases in a murine model,” Cryobiology, vol. 46, no. 3, pp. 238–245, 2003. View at Publisher · View at Google Scholar · View at Scopus
  72. C. Robert, L. Thomas, I. Bondarenko et al., “Ipilimumab plus dacarbazine for previously untreated metastatic melanoma,” The New England Journal of Medicine, vol. 364, no. 26, pp. 2517–2526, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. F. S. Hodi, S. J. O'Day, D. F. McDermott et al., “Improved survival with ipilimumab in patients with metastatic melanoma,” The New England Journal of Medicine, vol. 363, no. 8, pp. 711–723, 2010. View at Publisher · View at Google Scholar · View at Scopus
  74. J. S. Weber, S. O'Day, W. Urba et al., “Phase I/II study of ipilimumab for patients with metastatic melanoma,” Journal of Clinical Oncology, vol. 26, no. 36, pp. 5950–5956, 2008. View at Publisher · View at Google Scholar · View at Scopus
  75. J. C. Yang, M. Hughes, U. Kammula et al., “Ipilimumab (anti-CTLA4 antibody) causes regression of metastatic renal cell cancer associated with enteritis and hypophysitis,” Journal of Immunotherapy, vol. 30, no. 8, pp. 825–830, 2007. View at Publisher · View at Google Scholar · View at Scopus
  76. A. J. M. van den Eertwegh, J. Versluis, H. P. van den Berg et al., “Combined immunotherapy with granulocyte-macrophage colony-stimulating factor-transduced allogeneic prostate cancer cells and ipilimumab in patients with metastatic castration-resistant prostate cancer: a phase 1 dose-escalation trial,” The Lancet Oncology, vol. 13, no. 5, pp. 509–517, 2012. View at Publisher · View at Google Scholar · View at Scopus
  77. B. C. Carthon, J. D. Wolchok, J. Yuan et al., “Preoperative CTLA-4 blockade: tolerability and immune monitoring in the setting of a presurgical clinical trial,” Clinical Cancer Research, vol. 16, no. 10, pp. 2861–2871, 2010. View at Publisher · View at Google Scholar · View at Scopus
  78. F. S. Hodi, M. Butler, D. A. Oble et al., “Immunologic and clinical effects of antibody blockade of cytotoxic T lymphocyte-associated antigen 4 in previously vaccinated cancer patients,” Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 8, pp. 3005–3010, 2008. View at Publisher · View at Google Scholar · View at Scopus
  79. J. R. Brahmer, S. S. Tykodi, L. Q. M. Chow et al., “Safety and activity of anti-PD-L1 antibody in patients with advanced cancer,” The New England Journal of Medicine, vol. 366, no. 26, pp. 2455–2465, 2012. View at Publisher · View at Google Scholar · View at Scopus
  80. T. Powles, J. P. Eder, G. D. Fine et al., “MPDL3280A (anti-PD-L1) treatment leads to clinical activity in metastatic bladder cancer,” Nature, vol. 515, no. 7528, pp. 558–562, 2014. View at Publisher · View at Google Scholar
  81. S. L. Topalian, F. S. Hodi, J. R. Brahmer et al., “Safety, activity, and immune correlates of anti-PD-1 antibody in cancer,” The New England Journal of Medicine, vol. 366, no. 26, pp. 2443–2454, 2012. View at Publisher · View at Google Scholar · View at Scopus
  82. A. Machlenkin, O. Goldberger, B. Tirosh et al., “Combined dendritic cell cryotherapy of tumor induces systemic antimetastatic immunity,” Clinical Cancer Research, vol. 11, no. 13, pp. 4955–4961, 2005. View at Publisher · View at Google Scholar · View at Scopus
  83. M. H. M. G. M. den Brok, R. P. M. Sutmuller, S. Nierkens et al., “Synergy between in situ cryoablation and TLR9 stimulation results in a highly effective in vivo dendritic cell vaccine,” Cancer Research, vol. 66, no. 14, pp. 7285–7292, 2006. View at Publisher · View at Google Scholar · View at Scopus
  84. P. Redondo, J. del Olmo, A. López-Diaz de Cerio et al., “Imiquimod enhances the systemic immunity attained by local cryosurgery destruction of melanoma lesions,” Journal of Investigative Dermatology, vol. 127, no. 7, pp. 1673–1680, 2007. View at Publisher · View at Google Scholar · View at Scopus
  85. S. Nierkens, M. H. den Brok, T. Roelofsen et al., “Route of administration of the TLR9 agonist CpG critically determines the efficacy of cancer immunotherapy in mice,” PLoS ONE, vol. 4, no. 12, Article ID e8368, 2009. View at Publisher · View at Google Scholar · View at Scopus
  86. Q. Liu, B. Zhai, W. Yang et al., “Abrogation of local cancer recurrence after radiofrequency ablation by dendritic cell-based hyperthermic tumor vaccine,” Molecular Therapy, vol. 17, no. 12, pp. 2049–2057, 2009. View at Publisher · View at Google Scholar · View at Scopus
  87. R. Waitz, S. B. Solomon, E. N. Petre et al., “Potent induction of tumor immunity by combining tumor cryoablation with anti-CTLA-4 therapy,” Cancer Research, vol. 72, no. 2, pp. 430–439, 2012. View at Publisher · View at Google Scholar · View at Scopus
  88. A. Thakur, P. Littrup, E. N. Paul, B. Adam, L. K. Heilbrun, and L. G. Lum, “Induction of specific cellular and humoral responses against renal cell carcinoma after combination therapy with cryoablation and granulocyte-macrophage colony stimulating factor: a pilot study,” Journal of Immunotherapy, vol. 34, no. 5, pp. 457–467, 2011. View at Publisher · View at Google Scholar · View at Scopus
  89. L. Niu, J. Chen, L. He et al., “Combination treatment with comprehensive cryoablation and immunotherapy in metastatic pancreatic cancer,” Pancreas, vol. 42, no. 7, pp. 1143–1149, 2013. View at Publisher · View at Google Scholar · View at Scopus
  90. A. Zerbini, M. Pilli, A. Penna et al., “Radiofrequency thermal ablation of hepatocellular carcinoma liver nodules can activate and enhance tumor-specific T-cell responses,” Cancer Research, vol. 66, no. 2, pp. 1139–1146, 2006. View at Publisher · View at Google Scholar · View at Scopus
  91. G. Schueller, J. Kettenbach, R. Sedivy et al., “Heat shock protein expression induced by percutaneous radiofrequency ablation of hepatocellular carcinoma in vivo,” International Journal of Oncology, vol. 24, no. 3, pp. 609–613, 2004. View at Google Scholar · View at Scopus
  92. C. Napoletano, F. Taurino, M. Biffoni et al., “RFA strongly modulates the immune system and anti-tumor immune responses in metastatic liver patients,” International Journal of Oncology, vol. 32, no. 2, pp. 481–490, 2008. View at Google Scholar · View at Scopus
  93. A. Zerbini, M. Pilli, D. Laccabue et al., “Radiofrequency thermal ablation for hepatocellular carcinoma stimulates autologous NK-cell response,” Gastroenterology, vol. 138, no. 5, pp. 1931–1942.e2, 2010. View at Publisher · View at Google Scholar · View at Scopus
  94. M. H. M. G. M. den Brok, R. P. M. Sutmuller, R. van der Voort et al., “In situ tumor ablation creates an antigen source for the generation of antitumor immunity,” Cancer Research, vol. 64, no. 11, pp. 4024–4029, 2004. View at Publisher · View at Google Scholar · View at Scopus
  95. R. Rai, C. Richardson, P. Flecknell, H. Robertson, A. Burt, and D. M. Manas, “Study of apoptosis and heat shock protein (HSP) expression in hepatocytes following radiofrequency ablation (RFA),” Journal of Surgical Research, vol. 129, no. 1, pp. 147–151, 2005. View at Publisher · View at Google Scholar · View at Scopus
  96. N. Bhardwaj, J. Dormer, F. Ahmad et al., “Heat shock protein 70 expression following hepatic radiofrequency ablation is affected by adjacent vasculature,” Journal of Surgical Research, vol. 173, no. 2, pp. 249–257, 2012. View at Publisher · View at Google Scholar · View at Scopus
  97. S. Osada, H. Imai, H. Tomita et al., “Serum cytokine levels in response to hepatic cryoablation,” Journal of Surgical Oncology, vol. 95, no. 6, pp. 491–498, 2007. View at Publisher · View at Google Scholar
  98. T. Si, Z. Guo, and X. Hao, “Immunologic response to primary cryoablation of high-risk prostate cancer,” Cryobiology, vol. 57, no. 1, pp. 66–71, 2008. View at Publisher · View at Google Scholar · View at Scopus
  99. M. Udagawa, C. Kudo-Saito, G. Hasegawa et al., “Enhancement of immunologic tumor regression by intratumoral administration of dendritic cells in combination with cryoablative tumor pretreatment and Bacillus Calmette-Guerin cell wall skeleton stimulation,” Clinical Cancer Research, vol. 12, no. 24, pp. 7465–7475, 2006. View at Publisher · View at Google Scholar · View at Scopus