The interrelationship between cryoablation, the immune response and the tumor microenvironment: Stimulatory and suppressive effects

Tumor Ablation: Effects on Systemic and Local Anti-Tumor Immunity and on Other Tumor-Microenvironment Interactions

Volumn , Issue , 2013, Pages 77-107

  Sabel, Michael S ^a,b  

^a UNIVERSITY OF MICHIGAN COMPREHENSIVE CANCER CENTER   (United States)

^b Division of Surgical Oncology   (United States)

Author keywords

Apoptosis; Cryoablation; Cryoimmunology; Cryosurgery; Cytokines; Danger signals; Danger theory; Dendritic cells; Immune response; Immune suppression; In situ ablation; Macrophage activation; Membrane damage; Necrosis; Regulatory T cells; Tumor microenvironment

Indexed keywords

EID: 84891864640     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-94-007-4694-7_5     Document Type: Chapter

References (144)

1. Breasted JH (1930) The Edwin Smith surgical papyrus, Vol III. University of Chicago, Oriental Institute Publications, Chicago, pp 72-73
2. Korpan NN (2007) A history of cryosurgery: It’s development and future. JACS 204:314-324
3. Bird HM, Arnott James, MD (Aberdeen) (1949) 1797-1883. A pioneer in refrigeration analgesia. Anaesthesia 4:10-17
4. Campbell-White A (1899) Liquid Air: it’s application in medicine and surgery. Med Rec 56:109-112
5. Allington HV (1950) Liquid nitrogen in the treatment of skin diseases. CalifMed72:153-155
6. Crisp WE, Asadourian L, Romberger W (1960) Application of cryosurgery to gynecologic malignancy. Obstet Gynecol 30:668
7. Cooper IS (1963) Cryogenic surgery: a new method of destruction or extirpation of benign or malignant tissues. NEJM 268:743-749
8. Cooper IS, Lee A (1961) Cryostatic congelation: a system for producing a limited controlled region of cooling or freezing of biologic tissues. J Nerv Ment Dis 133:259-263
9. Kokoszka A, Sceinfeld N (2003) Evidence-based review of the use of cryosurgery in treatment of basal cell carcinoma. Dermatol Surg 29:566-571
10. Levy D, Avallone A, Jones JS (2010) Current state of urological cryosurgery: prostate and kidney. BJU Int 105:590-600
11. Ritch CR, Katz AE (2009) Prostate cryotherapy: current status. Curr Opin Urol 19:177-181
12. Venkatesan AM, Wood BJ, Gervais DA (2011) Percutaneous ablation in the kidney. Radiology 261:375-391
13. Bhardwaj N, Strickland AD, Dennison AF, Lloyd DM (2010) Liver ablation techniques: a review. Surg Endosc 24:254-265
14. Sotsky TK, Ravikumar TS (2002) Cryotherapy in the treatment of liver metastases from colorectal cancer. Semin Oncol 29:183-191
15. Littrup PJ, Jallad B, Chandiwala-Mody P et al (2009) Cryotherapy for breast cancer: A feasibility study without excision. J Vasc Interv Radiol 20:1329-1341
16. Sabel MS, Kaufman CS, Whitworth P et al (2004) Cryoablation of early-stage breast cancer: work-in-progress report of a multi-institutional trial. Ann Surg Oncol 11:542-549
17. Lee SH, Choi WJ, Sung SW et al (2011) Endoscopic cryotherapy of lung and bronchial tumors: a systematic review. Korean J Internal Med 26:137-144
18. Pau BB, Thornton RH, Solomon SB (2010) Ablationof pulmonary malignancy: current status. J Vasc Interv Radiol 21:S223-232
19. Callstrom MR, Kurup AN (2009) Percutaneous ablation for bone and soft tissue metastases-why cryoablation? Skeletal Radiol 38:835-839
20. Rybak LD (2009) Fire and ice: thermal ablation of musculoskeletal tumors. Radiol Clin North Am 47:455-469
21. Ablin RJ, Soanes WA, Conder MJ (1971a) Prospects for cryo-immunotherapy in cases of metastasizing carcinoma of the prostate. Cryobiology 8:271-279
22. Gursel E, Roberts M, Veenema RJ (1972) Regression of prostatic cancer following sequential cryotherapy to the prostate. J Urol 108:928-932
23. Soanes WA, Ablin RJ, Gonder MJ (1970) Remission of metatatic lesions following cryosurgery in prostatic cancer: Immunologic considerations. J Urol 104:154-159
24. Suzuki Y (1995) Cryosurgical treatment of advanced breast cancer and cryoimmunological responses. Skin Cancer 10:19-26
25. Tanaka S (1982) Immunological aspects of cryosurgery in general surgery. Cryobiology 19:247-262
26. Tanaka S (1995) Cryosurgical treatment of advanced breast cancer. Skin Cancer 10:9-18
27. Tramoyeres Cases A, Sanchez-Cuenca J, Tramoyeres Celma A, Beaumud G (1976) A la criocirugia transperineal en al tratamiento del cancer prostatico. Arch Espan Urol 29:119-142
28. Blackwood CE, Cooper IS (1972) Response of experimental tumor systems to cryosurgery. Cryobiology 9:508-515
29. Neel HBd, Ketcham AS, Hammond WG (1973) Experimental evaluation of in situ oncocide for primary tumor therapy: Comparison of tumor-specific immunity after complete excision cryonecrosis and ligation. Laryngoscope 83:376-387
30. Bagley DH, Faraci RP, Marrone JC, Beazley RM (1974) Lymphocyte mediated cytotoxicity after cryosurgery of a murine sarcoma. J Surg Res 17:404-406
31. Javadpour N, Bagley DH, Zbar B (1979) Failure of cryosurgical treatment of experimental intradermal tumors to eradicate microscopic lymph node metastases in guinea pigs. J Natl Cancer Inst 62:1479-1481
32. Misao A, Sakata K, Saji S, Kuneida T (1981) Late appearance of resistance to tumor rechallenge following cryosurgery: a study in an experimental mammary tumor of the rat. Cryobiology 18:386-389
33. Yamashita T, Hayakawa K, Hosokawa M et al (1982) Enhanced tumor metastases in rats following cryosurgery of primary tumor. Gan To Kagaku Ryoho 73:222-228
34. Hayakawa K, Yamashita T, Suzuki K et al (1982) Comparative immunological studies in rats following cryosurgery and surgical excision of 3-methylcholantrene-induced primary autochthousous tumors. Gann 73:462-469
35. Muller LC, Micksche M, Yamagata S, Kerschbaumer F (1985) Therapeutic effect of cryosurgery of murine osteosarcoma—Influence on disease outcome and immune function. Cryobiology 22:77-85
36. Wing MG, Rogers K, Jacob G, Rees RC (1988) Characterisation of suppressor cells generated following cryosurgery of an HSV-2-induced fibrosarcoma. Cancer Immunol Immunother 26:169-175
37. Shibata T, Suzuki K, Yamashita T et al (1998a) Immunological analysis of enhanced spontaneous metastasis in WKA rats following cryosurgery. Anticancer Res 18:2483-2486
38. Shibata T, Yamashita T, Suzuki K et al (1998c) Enhancement of experimental pulmonary metastasis and inhibition of subcutaneously transplanted tumor growth following cryosurgery. Anticancer Res 18:4443-4448
39. Horan AH (1975) Sequential cryotherapy for prostatic carcinoma: does it palliate the bone pain? Conn Med 39:81-83
40. Joosten JJA, van Muijen GNP, Whobbes T, Ruers TJM (2001) In vivo destruction of tumor tissue by cryoablation can induce inhibition of secondary tumor growth: an experimental study. Cryobiology 42(1):49-58
41. den Brok MHMGM, Sutmuller RPM, Nierkens S et al (2006a) Efficient loading of dendritic cells following cryo and radiofrequency ablation in combination with immune modulation induced anti-tumor immunity. Br J Cancer 95:896-905
42. Udagawa M, Kudo-Saito C, Gasegawa G, Yano K, Yamamoto A, Yaguchi M, Toda M, Azuma I, Iwai T, kawakami Y (2006) Enhancement of immunologic tumor regression by intratumoral administration of dendritic cells in combination with cryoablative tumor pretreatment and Bacillus Calmette-Guerin ceil wall skeleton stimulation. Clin Cancer Res 12:7465-75
43. Sabel MS, Nehs MA, Su G et al (2005) Immunologic response to cryoablation of breast cancer. Breast Cancer Res Treat 90:97-104
44. Machlenkin A, Goldberger O, Tirosh B et al (2005) Combined dendritic cell cryotherapy of tumor induces systemic antimetastatic immunity. Clin Cancer Res 11:4954-4961
45. Redondo P, del Olmo J, Lopez-Diaz de Cerio A et al (2007) Imiquimod enhances the systemic immunity attained by local cryosurgery destruction of melanoma lesions. J Invest Dermatol 127:1673-1680
46. Sabel MS, Su G, Griffith KA, Chang AE (2009) Rate of freeze alters the immunologic response after cryoablation of breast cancer. Ann Surg Oncol 17:1187-1193
47. Matin SF, Sharma P, Gill IS et al (2010) Immunological response to renal cryoablation in an in vivo orthotopic renal cell carcinoma murine model. Investig Urol183:333-338
48. Li M, Zhang S, Zhou Y et al (2010) Argon-helium cryosurgery for treatment of C6 gliomas in rats and its effect on cellular immunity. Technol Cancer Res Treat 9:87-93
49. Ablin RJ, Soanes WA, Gonder MJ (1973) Elution of in vivo bound antiprostatic epithelial antibodies following multiple cryotherapy of carcinoma of prostate. Urology 11:276-279
50. Huang FP, Platt N, Wykes M et al (2000) A discrete subpopulation of dendritic cells transports apoptotic intestinal epithelial cells to T-cell areas of mesenteric lymph nodes. J Exp Med 191:435-444
51. Ulschmid G, Kolb E, Largiader F (1979) Cryosurgery of pulmonary metastases. Cryobiology 16:171-178
52. Ablin RJ, Sadoughi N, Guinan P, Bruns GR, Bush IM (1977) Biphasic effect of cryosurgery of the prostate on lymphocyte proliferation. Cryobiology 14:60-67
53. Erinjeri JP, Clark TWI (2010) Cryoablation: Mechanism of action and devices. J Vasc Interv Radiol 21:S187-191
54. Hoffman NE, Bischof JC (2002) The cryobiology of cryosurgical injury. Urology 60:40-49
55. Mazur P (1984) Freezing of living cells: mechanisms and implications. Am J Physiol 247:C125-142
56. Mazur P, Rall WF, Leibo SP (1984) Kinetics of water loss and the likelihood of intracellular freezing in mouse ova Influence of the method of calculating the temperature dependence of water permeability. Cell Biophys 6:197-213
57. Bryant G (1995) Measurment of cell suspensions during successive freezing runs: implications for the mechanisms of intracellular ice formation. Cryobiology 32:114-128
58. Chapman WC, Debelak JP, Pinson CW et al (2000b) Hepatic cryoablation, but not radiofrequency ablation, results in lung inflammation. Ann Surg 231:752-761
59. Baust JG, Gage AA (2005) The molecular basis of cryosurgery. BJU Int 95:1187-1191
60. Gage AA, Baust J (1998) Mechanisms of tissue injury in cryosurgery. Cryobiology 37:171-186
61. Clarke DM, Robilotto AT, Rhee E et al (2007) Cryoablation of renal cancer: variables involved in freezing-induced cell death. Technol Cancer Res Treat 6:69-79
62. Wen J, Duan Y, Zou Z et al (2007) Cryoablation induces necrosis and apoptosis in lung adenocarcinoma in mice. Technol Cancer Res Treat 6:635-640
63. Hanai A, Yang W, Ravikumar TS (2001) Induction of apoptosis in human colon carcinoma cells TH29 by sublethal cryo-injury: Mediation by cytochrome c release. Int J Cancer 93:526-533
64. Yang W, Addona T, Nair DG, Qi L, Ravikumar TS (2003) Apoptosis induced by cryo-injury in human colorectal cancer cells is associated with mitochondrial dysfunction. Int J Cancer 103:360-369
65. Forest V, Peoc’h M, Campos L, Guyotat D, Vergnon JM (2006) Benefit of a combined treatment of cryotherapy and chmotherapy on tumor growth and late cryo-induced angiogenesis in a non-small cell lung cancer model. Lung Cancer 54:79-86
66. Steinbach JP, Weissenberger J, Aguzzi A (1999) Disteince phases of cryogenic tissue damage in the cerebral cortex of wild-type and c-fos deficient mice. Neuropathol Appl Neurbiol 25:468-480
67. Finelli A, Rewcastle JC, Jewett MA (2003) Cryotherapy and radiofrequency ablation: patholphysiologic basis and laboratory studies. Curr Opin Urol 13:187-191
68. Weber SM, Lee FT, Chinn DO et al (1997) Perivascular and intralesional tissue necrosis after hepatic cryoablation: results in a porcine model. Surgery 122:742-747
69. Viorritto ICB, Nikolov NP, Siegel RM (2007) Autoimmunity versus tolerance: Can dying cells tip the balance? Clin Immunol 122:125-134
70. Skoberne M, Beignon AS, Bhardwaj N (2004) Danger signals: a time and space continuum. Trends Mol Med 10:251-257
71. Demaria S, Bhardwaj N, McBride WH, Formenti SC (2005) Combining radiotherapy and immunotherapy: A revived partnership. Int J Radiat Oncol Biol Phys 63:655-666
72. Okamura Y, Watari M, Jerud ES et al (2002) The extra domain A of fibronectin activates Toll-like receptor 4. J Biol Chem 276:10229-10233
73. Smiley ST, King JA, Hancock WW (2001) Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. J Immunol 167:2887-2894
74. Termeer C, Benedix F, Sleeman J et al (2002) Oligosaccharides of hyaluronan activate dendritic cells via toll-like receptor 4. J Exp Med 195:99-111
75. Gallucci S, Lolkema M, Matzinger P (1999) Natural adjuvants: endogenous activators of dendritic cells. Nat Med 5:1249-1255
76. Sauter B, Albert ML, Francisco L et al (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 191:423-434
77. Peng Y, Martin DA, Kenkel J et al (2007) Innate and adaptive immune response to apoptotic cells. J Autoimmun 29:303-309
78. Scheinecker C, McHugh R, Shevach EM, Germain RN (2002) Constitutive presentation of a natural tissue autoantigen exclusively by dendritic cells in the draining lymph node. J Exp Med 196:1079-1090
79. Fadok VA, Bratton DL, Konowal A et al (1998) Macrophages that have ingested apoptotic cells in vitro inhibit proinflammatory cytokine production through autocrine/paracrine mechanisms involving TGF-beta PGE2 and PAF. J Clin Invest 101:890-898
80. Savill J, Dransfield I, Gregory C, Haslett C (2002) A blast from the past: clearance of apoptotic cells regulates immune responses. Nat Rev Immunol 2:965-975
81. Liu K, Iyoda T, Saternus M et al (2002) Immune tolerance after delivery of dying cells to dendritic cells in situ. J Exp Med 196:1091-1097
82. Stuart LM, Lucas M, Simpson C, Lamb J, Savill J, Lacy-Hulbert A (2002) Inhibitory effects of apoptotic cell ingestion upon endotoxin-driven myeloid dendritic cell maturation. J Immunol 168:1627-1635
83. Fuchs EJ, Matzinger P (1996) Is cancer dangerous to the immune system? Semin Immunol 8:271-280
84. Matzinger P (1994) Tolerance danger and the extended family. Annu Rev Immunol 12:991-1045
85. Henry F, Boisteau O, Bretaudeau L et al (1999) Antigen-presenting cells that phagocytose apoptotic tumor-derived cells are potent tumor vaccines. Cancer Res 59:3329-3332
86. Rock KL, Hearn A, Chen CJ et al (2005) Natural endogenous adjuvants. Springer Semin Immunopathol 26:231-246
87. Scheffer SR, Nave H, Korangy F et al (2003) Apoptotic but not necrotic tumor cell vaccines induce a potent immune response in vivo. Int J Cancer 103:205-211
88. Reddy KP, Ablin RJ(1979) Immunologic and morphologic effects of cryosurgery of the monkey (Macaque) prostate. Res Exp Med 175:123-128
89. Schnurr M, Scholz C, Rothenfusser S et al (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 62:2347-2352
90. Jenne L, Arrighi JF, Jonuleit H, Saurat JH, Hauser C (2000) Dendritic cells containing apoptotic melanoma cells primar human CD8 + T cells for efficient tumor cell lysis. Cancer Res 60:4446-4452
91. Rovere P, Vallinoto C, Bondanza A et al (1998) Cutting edge: by-stander apoptosis triggers dendritic cells maturation and antigen-presenting function. J Immunol 161:4467-4471
92. Gage AA, Baust JM, Baust JG (2009) Experimental cryosurgery investigations in vivo. Cryobiology 59:229-243
93. Mazur P (1968) Physical-chemical factors underlying cell injury in cryosurgical freezing. In: Rand R, Rinfret A, von Leden H (eds) Cryosurgery. Charles C Thomas, Springfield, IL, pp 32-51
94. Bischof J, Christov K, Rubinsky B (1993) A morphological study of cooling rate response in normal and noeplastic human liver tissue: cryosurgical implications. Cryobiology 30:482-492
95. Hoffmann NE, Coad JE, Huot CS, Swanlund DJ, Bischoff JC (2001) Investigation of the mechanism and the effect of cryoimmunology in the Copenhagen rat. Cryobiology 41:59-68
96. Gage AA, Guest K, Montes M, Caruana JA, Whalen DA (1985) Effect of varying freezing and tawing rates in experimental cryosurgery. Cryobiology 22:175-182
97. Neel HB, DeSanto LW (1973) Cryosurgical control of cancer: effets of freeze rates tumor temperatures and ischemia. Ann Otol Rhinol Laryngol 82:716-723
98. Cahan WG (1965) Cryosurgery of malignant and benign tumors. Fed Proc 24:S241-248
99. Cooper IS (1965) Cryogenic surgery for cancer. Fed Proc 24:S237-240
100. Gage AA, Koepf S, Whehrle D, Emmings F (1965) Cryotherapy for cancer of the lip and oral cavity. Cancer 18:1646-1651
101. Whittaker DK (1975) Repeat freeze cycles in cryosurgery of oral tissues. Br Dent J 139:459-465
102. Ablin RJ (1974) Cryosurgery of the rabbit prostate: comparison of the immune response of immature and mature bucks. Cryobiology 11:416-422
103. Ablin RJ (1976) Cryosurgery of the monkey (Macaque) prostate. Cryobiology 13:47-53
104. Ablin RJ, Witebsky E, Jagodzinski RV, Soanes WA (1971b) Secondary immunologic response as a consequence of the in situ freezing of rabbit male adenexal glands tissues of reproduction. Exp Med Surg 29:72-88
105. Brandt EJ, Riera CM, Orsini F, Shulman S (1967) Cryoimmunology: the booster phenomenon. Cryobiology 3:382
106. Riera CM, Brandt EJ, Shulman S (1968) Studies in cryo-immunology IV: Antibody development in rabbits after iso-immunization followed by freezing. Immunology 15:779-787
107. Shulman S, Brandt EJ, Yantorno C (1968a) Studies in cryo-immunology. II: Tissue and species specificity of the autoantibody response and comparison to isoimmunoziation. Immunology 14:149-158
108. Shulman S, Bronson P, Riera CM, Brandt EJ, Yantorno C (1968b) Studies in cryoimmunology. III: The immunoglobulin nature of the antibody response. Immunology 14:541-551
109. Eastham RJ, Mason JM, Jennings BR, Bel ew PW, Maguda, TA (1976) T-cell rosette test in squamous cell carcinoma of the head and neck. Arch Otolaryngol 102:171-175
110. Fazio M, Airoldi M, Gandolfo S et al (1982a) Humoral and cellular immune response to cryosurgery of benign and malignant lesions of the oral cavity [Italian]. Bollettino Soc Ital Biol Sper 58:412-418
111. Fazio M, Airoldi M, Mastromatteo V et al (1982b) Cryosurgery as a stimulator of the host’s immune defences in benign and malignant oral cavity tumours. Panminerva Med 24:195-201
112. Kogel H, Grundmann R, Fohlmeister I, Pichlmaier H (1985) Cryotherapy of rectal cancer Immunologic results [German]. Zentralblatt fur Chirugie 110:147-154
113. Wang ZS (1989) Cryosurgery in rectal carcinoma report of 41 cases [Chinese]. Chinese J Oncol 11:226-227
114. Ravindranath MH, Wood TF, Soh D et al (2002) Cryosurgical ablation of liver tumors in colon cancer patients increases the serum total ganglioside level and then selectively augments antiganglioside IgM. Cryobiology 45:10-21
115. Si T, Guo Z, Hao X (2008) Immunologic response to primary cryoablation of high-risk prostate cancer. Cryobiology 57:66-71
116. Si TG, Guo Z, Wang HT et al (2009) Cryoablation for prostate cancer induces tumor-specific immune repsonse [Chinese]. Zhonghua Nan Ke Xue 15:350-353
117. Thakur A, Littrup P, Paul EN, Adam B, Heilbrun LK, Lum LG (2011) Induction of specific cellular and humoral responses against renal cell carcinoma after combination therapy with cryoablation and graunolcyte-macrophage colony stimulating factor: a pilot study. J Immunother 34:457-467
118. Friedman EJ, Orth CR, Brewton KA, Ponniah S, Alexander RB (1997) Cryosurgical ablation of the normal ventral prostate plus adjuvant does not protect Copenhagen rats from Dunning prostatic adenocarcinoma challenge. J Urol 158:1585-1588
119. Lubaroff DM, Reynolds CW, Canfield L et al (1981) Immunologic aspects of the prostate. Prostate 2:233-248
120. 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. J Jpn Surg Soc 94:57-65
121. Miya K, Saji S, Morita T, Niwa H, Sakata K (1987) Experimental study on mechanism of absorption of cryonecrotized tumor antigens. Cryobiology 24:135-139
122. Shibata T, Yamashita T, Suzuki K et al (1998b) Enhancement of experimental pulmonary metastaseis and inhibition of subcutaneously transplanted tumor growth following cryosurgery. Anticancer Res 18:4443-4448
123. Miha K, Saji S, Morita T et al (1986) Immunological response of regional lymph nodes after tumor cryosurgery: Experimental study in rats. Cryobiology 23:290-295
124. Urano M, Tanaka C, Sugiyama T, 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 46:238-245
125. Blackwell TS, Debelak JP, Venkatakrishnan A et al (1999) Acute lung injury after hepatic cryoablation: correlation with NF-κB activation and cytokine production. Surgery 126:518-526
126. Seifert JK, France MP, Zhao J et al (2002) Large volume hepatic freezing: association with significant release of the cytokines interleukin-6 and tumor necrosis factor alpha in a rat model. World J Surg 26:1333-1341
127. Wudel LJ Jr, Allos TM, Washington MK, Sheller JR, Chapman WC (2003) Multi-organ inflammation after hepatic cryoablation in BALB/c mice. J Surg Res 12(2):131-137
128. Ng KK, Lam CM, Poon RT et al (2004) Comparison of systemic responses of radiofrequency ablation, cryoablation and surgical resection in a porcine liver model. Ann Surg Oncol 11:650-657
129. Seifert JK, Stewart GJ, Hewitt PM et al (1999) Interleukin-6 and tumor necrosis factor-alpha levels following hepatic cryotherapy: association with volume and duration of freezing. World J Surg 23:1019-1026
130. de Jong KP, von Geausau BA, Rottier CA, Bijzet J, Limburg PC, de Vries EGE, Fidler V, Sloof MJH (2001) Serum response of hepatocyte growth factor, insulin like growth factor, interleukin 6, and acute phase proteins in patients with colorectal liver metastases treated with partial hepatectomy or cryosurgery. Journal of Hepatology 34(3):422-427
131. Osada S, Yoshida K, Saji S (2009) A novel strategy by cryoablation for advanced hepatoma. Anticancer Res 29:5203-5210
132. Osada S, Imai H, Tomita H et al (2007) Serum cytoine levels in response to hepatic cryoablation. J Surg Oncol 95:491-498
133. Chapman WC, Debelak JP, Blackwell TS et al (2000a) Hepatic cryoablation-induced acute lung injury: pulmonary hemodynamic and permeability effects in a sheep model. Arch Surg 135:667-672
134. Jansen MC, van Hillegersberg R, Schoots IG et al (2010) Cryoablation induceds greaterinflam-matory and coagulative responses than radiofrequency ablation or laser induced thermotherapy in a rat liver model. Surgery 147:686-695
135. Nishida H, Yamamoto N, Tanzawa Y, Tsuchiya H (2011) Cryoimmunology for malignant bone and soft-tissue tumors. Int J Clin Oncol 16:109-117
136. Gazzaniga S, Bravo A, Goldszmid SR et al (2001) Inflammatory changes after cryosurgery-induced necrosis in human melanoma xenografted in nude mice. J Invest Dermatol 116:664-671
137. Sabel MS, Arora A, Su G, Chang AE (2006) Adoptive immunotherapy of breast cancer with lymph node cells primed by cryoablation of the primary tumor. Cryobiology 53:360-366
138. Renziehausen K, Schroder M, Seeber C, Krafft W, Kleinschmidt R (1975) Immunologic studies in relation to cryotherapy of gynecologic diseases. Zentralblatt fuer Gynaekologie 97:1492-1501
139. Weyer U, Peterson I, Ehrke C, Carstensen A, Nussgen A, Russ C, Gottsch B, Kowalzick L, Arndt R, Breitbart EW (1989) Immunomodulation by cryosurgery in malignant melanoma [German]. Onkologie 12:291-296
140. Levy MY, Sidana A, Chowdhury WH et al (2009) Cyclophosphamide unmasks an antimetastatic effect of local tumor cryoablation. J Pharmacol Exp Therapeut 330:596-601
141. Si TG, Guo Z, Wang HT, Liu CF, Yang M (2011) Experimental study on the immune functions of splenic dendritic cells after a combined therapy of cryoablation and granulocyte macrophage-colon stimulating factor for prostate cancer. Zhongua Yi Zue Za Zhi 91:1184-1187
142. Ismail M, Morgan R, Harrington K, Davies J, Pahnda H (2010) Immunoregulatory effects of freeze injured whole tumor cells on human dendritic cells using an in vitro cryotherapy model. Cryobiology 61:268-274
143. den Brok HMGM, Sutmuller RPM, Nierkens S et al (2006b) Synergy between in situ cryosurgery and TLR9 stimulation results in a highly effective in vivo dendritic cell vaccine. Cancer Res 66:7285-7292
144. Nierkens S, Den Brok MH, Roelofsen T et al (2009) Route of administration of the TLR9 agonist CpG critically determines the effiacy of cancer immunotherapy in mice. PLos One 4:e8368