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The Interrelationship Between Cryoablation, the Immune Response and the Tumor Microenvironment: Stimulatory and Suppressive Effects

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Tumor Ablation

Part of the book series: The Tumor Microenvironment ((TTME,volume 5))

Abstract

Cryoablation involves the use of freezing temperatures to kill cells and destroy tissue. Its history as a cancer therapy dates back over 100 years, however recent advances in technology have greatly expanded its clinical potential. Much of the interest in cryoablation centers on early observations that after freezing a primary lesion, distant, un-treated sites of disease began to regress. It was believed that this was secondary to cryoablation stimulating an anti-tumor immune response. This prompted multiple pre-clinical studies examining the impact of cryoablation on the immune response and the mechanisms involved. While most of these studies validated the ability of cryoablation to stimulate tumor recognition by the immune system, some studies demonstrated the opposite; tumor-bearing animals treated by cryoablation had diminished responses and increased tumor growth compared to controls. As our knowledge of the components of the immune system and their interactions in the generation, or suppression, of an immune response has increased, as well as our understanding of the mechanisms by which freezing leads to cell death, the immunomodulation seen with cryoablation is becoming clearer. Many questions still remain, but given the tremendous clinical potential in having a local therapy that could also have systemic benefits, further research in this area is strongly warranted. This chapter will review the history of cryosurgery for the treatment of cancer, including the observations of distant tumor regression; detail the mechanisms by which cryoablation leads to cancer cell death, and how this can be altered by variations in cryosurgical technique; and describe the pre-clinical data examining the relationship between cryoablation-induced cell death and both stimulatory and suppressive immune responses.

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Reference

  1. Breasted JH (1930) The Edwin Smith surgical papyrus, Vol III. University of Chicago, Oriental Institute Publications, Chicago, pp 72–73

    Google Scholar 

  2. Korpan NN (2007) A history of cryosurgery: It’s development and future. JACS 204:314–324

    Google Scholar 

  3. Bird HM, Arnott James, MD (Aberdeen) (1949) 1797–1883. A pioneer in refrigeration analgesia. Anaesthesia 4:10–17

    Google Scholar 

  4. Campbell-White A (1899) Liquid Air: it’s application in medicine and surgery. Med Rec 56:109–112

    Google Scholar 

  5. Allington HV (1950) Liquid nitrogen in the treatment of skin diseases. Calif Med 72:153–155

    PubMed  CAS  Google Scholar 

  6. Crisp WE, Asadourian L, Romberger W (1960) Application of cryosurgery to gynecologic malignancy. Obstet Gynecol 30:668

    Google Scholar 

  7. Cooper IS (1963) Cryogenic surgery: a new method of destruction or extirpation of benign or malignant tissues. NEJM 268:743–749

    Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    PubMed  Google Scholar 

  10. Levy D, Avallone A, Jones JS (2010) Current state of urological cryosurgery: prostate and kidney. BJU Int 105:590–600

    PubMed  Google Scholar 

  11. Ritch CR, Katz AE (2009) Prostate cryotherapy: current status. Curr Opin Urol 19:177–181

    PubMed  Google Scholar 

  12. Venkatesan AM, Wood BJ, Gervais DA (2011) Percutaneous ablation in the kidney. Radiology 261:375–391

    PubMed  Google Scholar 

  13. Bhardwaj N, Strickland AD, Dennison AF, Lloyd DM (2010) Liver ablation techniques: a review. Surg Endosc 24:254–265

    PubMed  CAS  Google Scholar 

  14. Sotsky TK, Ravikumar TS (2002) Cryotherapy in the treatment of liver metastases from colorectal cancer. Semin Oncol 29:183–191

    PubMed  Google Scholar 

  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

    PubMed  Google Scholar 

  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

    PubMed  Google Scholar 

  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

    Google Scholar 

  18. Pau BB, Thornton RH, Solomon SB (2010) Ablation of pulmonary malignancy: current status. J Vasc Interv Radiol 21:S223–232

    Google Scholar 

  19. Callstrom MR, Kurup AN (2009) Percutaneous ablation for bone and soft tissue metastases- why cryoablation? Skeletal Radiol 38:835–839

    PubMed  Google Scholar 

  20. Rybak LD (2009) Fire and ice: thermal ablation of musculoskeletal tumors. Radiol Clin North Am 47:455–469

    PubMed  Google Scholar 

  21. Ablin RJ, Soanes WA, Conder MJ (1971a) Prospects for cryo-immunotherapy in cases of metastasizing carcinoma of the prostate. Cryobiology 8:271–279

    Google Scholar 

  22. Gursel E, Roberts M, Veenema RJ (1972) Regression of prostatic cancer following sequential cryotherapy to the prostate. J Urol 108:928–932

    PubMed  CAS  Google Scholar 

  23. Soanes WA, Ablin RJ, Gonder MJ (1970) Remission of metatatic lesions following cryosurgery in prostatic cancer: Immunologic considerations. J Urol 104:154–159

    PubMed  CAS  Google Scholar 

  24. Suzuki Y (1995) Cryosurgical treatment of advanced breast cancer and cryoimmunological responses. Skin Cancer 10:19–26

    Google Scholar 

  25. Tanaka S (1982) Immunological aspects of cryosurgery in general surgery. Cryobiology 19:247–262

    PubMed  CAS  Google Scholar 

  26. Tanaka S (1995) Cryosurgical treatment of advanced breast cancer. Skin Cancer 10:9–18

    Google Scholar 

  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

    Google Scholar 

  28. Blackwood CE, Cooper IS (1972) Response of experimental tumor systems to cryosurgery. Cryobiology 9:508–515

    PubMed  CAS  Google Scholar 

  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

    PubMed  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    CAS  Google Scholar 

  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

    CAS  Google Scholar 

  39. Horan AH (1975) Sequential cryotherapy for prostatic carcinoma: does it palliate the bone pain? Conn Med 39:81–83

    PubMed  CAS  Google Scholar 

  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

    Google Scholar 

  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

    Google Scholar 

  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 cell wall skeleton stimulation. Clin Cancer Res 12:7465–75

    PubMed  CAS  Google Scholar 

  43. Sabel MS, Nehs MA, Su G et al (2005) Immunologic response to cryoablation of breast cancer. Breast Cancer Res Treat 90:97–104

    PubMed  CAS  Google Scholar 

  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

    Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    PubMed  Google Scholar 

  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

    Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  51. Ulschmid G, Kolb E, Largiader F (1979) Cryosurgery of pulmonary metastases. Cryobiology 16:171–178

    Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  53. Erinjeri JP, Clark TWI (2010) Cryoablation: Mechanism of action and devices. J Vasc Interv Radiol 21:S187–191

    Google Scholar 

  54. Hoffman NE, Bischof JC (2002) The cryobiology of cryosurgical injury. Urology 60:40–49

    Google Scholar 

  55. Mazur P (1984) Freezing of living cells: mechanisms and implications. Am J Physiol 247:C125–142

    Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  57. Bryant G (1995) Measurment of cell suspensions during successive freezing runs: implications for the mechanisms of intracellular ice formation. Cryobiology 32:114–128

    PubMed  CAS  Google Scholar 

  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

    CAS  Google Scholar 

  59. Baust JG, Gage AA (2005) The molecular basis of cryosurgery. BJU Int 95:1187–1191

    PubMed  Google Scholar 

  60. Gage AA, Baust J (1998) Mechanisms of tissue injury in cryosurgery. Cryobiology 37:171–186

    PubMed  CAS  Google Scholar 

  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

    PubMed  Google Scholar 

  62. Wen J, Duan Y, Zou et al (2007) Cryoablation induces necrosis and apoptosis in lung adenocarcinoma in mice. Technol Cancer Res Treat 6:635–640

    PubMed  CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    PubMed  Google Scholar 

  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

    CAS  Google Scholar 

  67. Finelli A, Rewcastle JC, Jewett MA (2003) Cryotherapy and radiofrequency ablation: patholphysiologic basis and laboratory studies. Curr Opin Urol 13:187–191

    PubMed  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  69. Viorritto ICB, Nikolov NP, Siegel RM (2007) Autoimmunity versus tolerance: Can dying cells tip the balance? Clin Immunol 122:125–134

    PubMed  CAS  Google Scholar 

  70. Skoberne M, Beignon AS, Bhardwaj N (2004) Danger signals: a time and space continuum. Trends Mol Med 10:251–257

    PubMed  CAS  Google Scholar 

  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

    PubMed  Google Scholar 

  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

    Google Scholar 

  73. Smiley ST, King JA, Hancock WW (2001) Fibrinogen stimulates macrophage chemokine secretion through toll-like receptor 4. J Immunol 167:2887–2894

    PubMed  CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  75. Gallucci S, Lolkema M, Matzinger P (1999) Natural adjuvants: endogenous activators of dendritic cells. Nat Med 5:1249–1255

    PubMed  CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  77. Peng Y, Martin DA, Kenkel J et al (2007) Innate and adaptive immune response to apoptotic cells. J Autoimmun 29:303–309

    PubMed  CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  83. Fuchs EJ, Matzinger P (1996) Is cancer dangerous to the immune system? Semin Immunol 8:271–280

    PubMed  CAS  Google Scholar 

  84. Matzinger P (1994) Tolerance danger and the extended family. Annu Rev Immunol 12:991–1045

    PubMed  CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  86. Rock KL, Hearn A, Chen CJ et al (2005) Natural endogenous adjuvants. Springer Semin Immunopathol 26:231–246

    PubMed  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  88. Reddy KP, Ablin RJ(1979) Immunologic and morphologic effects of cryosurgery of the monkey (Macaque) prostate. Res Exp Med 175:123–128

    CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  92. Gage AA, Baust JM, Baust JG (2009) Experimental cryosurgery investigations in vivo. Cryobiology 59:229–243

    PubMed  CAS  Google Scholar 

  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

    Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    PubMed  Google Scholar 

  98. Cahan WG (1965) Cryosurgery of malignant and benign tumors. Fed Proc 24:S241–248

    Google Scholar 

  99. Cooper IS (1965) Cryogenic surgery for cancer. Fed Proc 24:S237–240

    Google Scholar 

  100. Gage AA, Koepf S, Whehrle D, Emmings F (1965) Cryotherapy for cancer of the lip and oral cavity. Cancer 18:1646–1651

    PubMed  CAS  Google Scholar 

  101. Whittaker DK (1975) Repeat freeze cycles in cryosurgery of oral tissues. Br Dent J 139:459–465

    PubMed  CAS  Google Scholar 

  102. Ablin RJ (1974) Cryosurgery of the rabbit prostate: comparison of the immune response of immature and mature bucks. Cryobiology 11:416–422

    PubMed  CAS  Google Scholar 

  103. Ablin RJ (1976) Cryosurgery of the monkey (Macaque) prostate. Cryobiology 13:47–53

    PubMed  CAS  Google Scholar 

  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

    CAS  Google Scholar 

  105. Brandt EJ, Riera CM, Orsini F, Shulman S (1967) Cryoimmunology: the booster phenomenon. Cryobiology 3:382

    Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    CAS  Google Scholar 

  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

    CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    CAS  Google Scholar 

  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

    CAS  Google Scholar 

  112. Kogel H, Grundmann R, Fohlmeister I, Pichlmaier H (1985) Cryotherapy of rectal cancer Immunologic results [German]. Zentralblatt fur Chirugie 110:147–154

    CAS  Google Scholar 

  113. Wang ZS (1989) Cryosurgery in rectal carcinoma report of 41 cases [Chinese]. Chinese J Oncol 11:226–227

    CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  115. Si T, Guo Z, Hao X (2008) Immunologic response to primary cryoablation of high-risk prostate cancer. Cryobiology 57:66–71

    PubMed  CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  119. Lubaroff DM, Reynolds CW, Canfield L et al (1981) Immunologic aspects of the prostate. Prostate 2:233–248

    PubMed  CAS  Google Scholar 

  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

    CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    CAS  Google Scholar 

  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

    Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    Google Scholar 

  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

    PubMed  Google Scholar 

  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

    Google Scholar 

  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

    Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    Google Scholar 

  131. Osada S, Yoshida K, Saji S (2009) A novel strategy by cryoablation for advanced hepatoma. Anticancer Res 29:5203–5210

    PubMed  CAS  Google Scholar 

  132. Osada S, Imai H, Tomita H et al (2007) Serum cytoine levels in response to hepatic cryoablation. J Surg Oncol 95:491–498

    PubMed  CAS  Google Scholar 

  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

    CAS  Google Scholar 

  134. Jansen MC, van Hillegersberg R, Schoots IG et al (2010) Cryoablation induceds greater inflammatory and coagulative responses than radiofrequency ablation or laser induced thermotherapy in a rat liver model. Surgery 147:686–695

    PubMed  Google Scholar 

  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

    PubMed  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    CAS  Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    CAS  Google Scholar 

  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

    Google Scholar 

  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

    PubMed  CAS  Google Scholar 

  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

    Google Scholar 

  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

    Google Scholar 

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Correspondence to Michael S. Sabel MD FACS .

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Sabel, M. (2013). The Interrelationship Between Cryoablation, the Immune Response and the Tumor Microenvironment: Stimulatory and Suppressive Effects. In: Keisari, Y. (eds) Tumor Ablation. The Tumor Microenvironment, vol 5. Springer, Dordrecht. https://doi.org/10.1007/978-94-007-4694-7_5

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