Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review
  • Published:

Re-purposing cryoablation: a combinatorial ‘therapy’ for the destruction of tissue

Abstract

It is now recognized that the tumor microenvironment creates a protective neo-tissue that isolates the tumor from the various defense strategies of the body. Evidence demonstrates that, with successive therapeutic attempts, cancer cells acquire resistance to individual treatment modalities. For example, exposure to cytotoxic drugs results in the survival of approximately 20–30% of the cancer cells as only dividing cells succumb to each toxic exposure. With follow-up treatments, each additional dose results in tumor-associated fibroblasts secreting surface-protective proteins, which enhance cancer cell resistance. Similar outcomes are reported following radiotherapy. These defensive strategies are indicative of evolved capabilities of cancer to assure successful tumor growth through well-established anti-tumor-protective adaptations. As such, successful cancer management requires the activation of multiple cellular ‘kill switches’ to prevent initiation of diverse protective adaptations. Thermal therapies are unique treatment modalities typically applied as monotherapies (without repetition) thereby denying cancer cells the opportunity to express defensive mutations. Further, the destructive mechanisms of action involved with cryoablation (CA) include both physical and molecular insults resulting in the disruption of multiple defensive strategies that are not cell cycle dependent and adds a damaging structural (physical) element. This review discusses the application and clinical outcomes of CA with an emphasis on the mechanisms of cell death induced by structural, metabolic, vascular and immune processes. The induction of diverse cell death cascades, resulting in the activation of apoptosis and necrosis, allows CA to be characterized as a combinatorial treatment modality. Our understanding of these mechanisms now supports adjunctive therapies that can augment cell death pathways.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Figure 1
Figure 2
Figure 3

Similar content being viewed by others

References

  1. Cooper IS, Lee AS . Cryostatic congelation: a system for producing a limited, controlled region of cooling or freezing of biologic tissues. J Nerv Ment Dis 1961; 133: 259–263.

    Article  CAS  PubMed  Google Scholar 

  2. Cooper IS . Cryobiology as viewed by the surgeon. Cryobiology 1964; 1: 44–51.

    Article  Google Scholar 

  3. Cooper IS . Cryogenic surgery for cancer. Fed Proc 1965; 24: S237–S240.

    CAS  PubMed  Google Scholar 

  4. Gage AA . Current status of cryosurgery for cancer. Compr Ther 1978; 4: 24–30.

    CAS  PubMed  Google Scholar 

  5. O'Donoghue EP, Milleman LA, Flocks RH, Culp DA, Bonney WW . Cryosurgery for carcioma of prostate. Urology 1975; 5: 308–316.

    Article  CAS  Google Scholar 

  6. Onik GM, Cohen JK, Reyes GD, Rubinsky B, Chang Z, Baust JG . Transrectal ultrasound-guided percutaneous radical cryosurgical ablation of the prostate. Cancer 1993; 72: 1291–1299.

    Article  CAS  PubMed  Google Scholar 

  7. Gage AA, Baust JG . Cryosurgery for tumors. J Am Coll Surg 2007; 205: 342–356.

    Article  PubMed  Google Scholar 

  8. Baust JG, Gage AA, Klossner DP, Clarke D, Miller R, Cohen J et al. Issues critical to the successful application of cryosurgical ablation of the prostate. Technol Cancer Res Treat 2007; 6: 97–109.

    Article  CAS  PubMed  Google Scholar 

  9. Chabner BA, Roberts TG Jr . Timeline: chemotherapy and the war on cancer. Nat Rev Cancer 2005; 5: 65–72.

    Article  CAS  PubMed  Google Scholar 

  10. Ghisolfi L, Keates AC, Hu X, Lee DK, Li CJ . Ionizing radiation induces stemness in cancer cells. PLoS One 2012; 7: e43628.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Sun Y, Campisi J, Higano C, Beer TM, Porter P, Coleman I et al. Treatment-induced damage to the tumor microenvironment promotes prostate cancer therapy resistance through WNT16B. Nat Med 2012; 18: 1359–1368.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Argyriou AA, Kyritsis AP, Makatsoris T, Kalofonos HP . Chemotherapy-induced peripheral neuropathy in adults: a comprehensive update of the literature. Cancer Manag Res 2014; 6: 135–147.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Gage AA, Baust JM, Baust JG . Experimental cryosurgery investigations in vivo. Cryobiology 2009; 59: 229–243.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Howlader N, Noone A, Krapcho M, Garshell J, Neyman N, Altekruse S et al. National Cancer Institute: SEER Cancer Statistics Review, 1975–2010 (based on November 2012 SEER data submission, posted to the SEER web site, April 2013). Available from http://seer.cancer.gov/csr/1975_2010/. Last accessed on 13 April 2013.

  15. Shackleton M, Quintana E, Fearon ER, Morrison SJ . Heterogeneity in cancer: cancer stem cells versus clonal evolution. Cell 2009; 138: 822–829.

    Article  CAS  PubMed  Google Scholar 

  16. Bonnet D, Dick JE . Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat Med 1997; 3: 730–737.

    Article  CAS  PubMed  Google Scholar 

  17. Hanahan D, Coussens LM . Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell 2012; 21: 309–322.

    Article  CAS  PubMed  Google Scholar 

  18. Hanahan D, Weinberg RA . Hallmarks of cancer: the next generation. Cell 2011; 144: 646–674.

    Article  CAS  PubMed  Google Scholar 

  19. Togo S, Polanska U, Horimoto Y, Orima A . Carcinoma-associated fibroblasts are a promising therapeutic target. Cancers 2013; 5: 149–169.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Jones JS . Radiorecurrent prostate cancer: an emerging and largely mismanaged epidemic. Eur Urol 2011; 60: 411–412.

    Article  PubMed  Google Scholar 

  21. Corn PG . The tumor microenvironment in prostate cancer: elucidating molecular pathways for therapy development. Cancer Manag Res 2012; 4: 183–193.

    Article  PubMed  PubMed Central  Google Scholar 

  22. Moltzahn F, Thalmann GN . Cancer stem cells in prostate cancer. Transl Androl Urol 2013; 2: 242–253.

    PubMed  PubMed Central  Google Scholar 

  23. Babaian RJ, Donnelly B, Bahn D, Baust JG, Dineen M, Ellis D et al. Best practice statement on cryosurgery for the treatment of localized prostate cancer. J Urol 2008; 180: 1993–2004.

    Article  PubMed  Google Scholar 

  24. Bischof J, Christov K, Rubinsky B . A morphological study of cooling rate response in normal and neoplastic human liver tissue: cryosurgical implications. Cryobiology 1993; 30: 482–492.

    Article  CAS  PubMed  Google Scholar 

  25. Bischof JC, Bastacky J, Rubinsky B . An analytical study of cryosurgery in the lung. J Biomech Eng 1992; 114: 467–472.

    Article  CAS  PubMed  Google Scholar 

  26. Robilotto AT, Baust JM, Van Buskirk RG, Gage AA, Baust JG . Temperature-dependent activation of differential apoptotic pathways during cryoablation in a human prostate cancer model. Prostate Cancer Prostatic Dis 2013; 16: 41–49.

    Article  CAS  PubMed  Google Scholar 

  27. Onik G, Porterfield B, Rubinsky B, Cohen J . Percutaneous transperineal prostate cryosurgery using transrectal ultrasound guidance: animal model. Urology 1991; 37: 277–281.

    Article  CAS  PubMed  Google Scholar 

  28. Onik G, Rubinsky B, Zemel R, Weaver L, Diamond D, Cobb C et al. Ultrasound-guided hepatic cryosurgery in the treatment of metastatic colon carcinoma. Preliminary results. Cancer 1991; 67: 901–907.

    Article  CAS  PubMed  Google Scholar 

  29. Baust JM, Snyder KK, Santucci KL, Robilotto AT, Smith J, McKain J et al. Assessment of SCN and argon cryoablation devices in an in vivo-like 3-D tissue engineered prostate and renal cancer model. Cryobiology 2014; 69: 198 (abstract).

    Google Scholar 

  30. Robilotto AT, Van Buskirk RG, Gage AA, Baust JM, Baust JG . Development of a tissue engineered human prostate tumor equivalent: evaluation of cryoablative techniques. Cryobiology 2013; 66: 354–355 (abstract).

    Google Scholar 

  31. Gage AA, Baust J . Mechanisms of tissue injury in cryosurgery. Cryobiology 1998; 37: 171–186.

    Article  CAS  PubMed  Google Scholar 

  32. Klossner DP, Baust JM, Van Buskirk RG, Gage AA, Baust JG . Cryoablative response of prostate cancer cells is influenced by androgen receptor expression. BJU Int 2008; 101: 1310–1316.

    Article  CAS  PubMed  Google Scholar 

  33. Smith DJ, Fahssi WM, Swanlund DJ, Bischof JC . A parametric study of freezing injury in AT-1 rat prostate tumor cells. Cryobiology 1999; 39: 13–28.

    Article  CAS  PubMed  Google Scholar 

  34. Klossner DP, Robilotto AT, Clarke DM, Van Buskirk RG, Baust JM, Gage AA et al. Cryosurgical technique: assessment of the fundamental variables using human prostate cancer model systems. Cryobiology 2007; 55: 189–199.

    Article  PubMed  Google Scholar 

  35. Baust JG, Gage AA . The molecular basis of cryosurgery. BJU Int 2005; 95: 1187–1191.

    Article  PubMed  Google Scholar 

  36. Rodriguez-Bigas MA, Klippenstein D, Meropol NJ, Weber TK, Petrelli NJ . A pilot study of cryochemotherapy for hepatic metastases from colorectal cancer. Cryobiology 1996; 33: 600–606.

    Article  CAS  PubMed  Google Scholar 

  37. Clarke DM, Baust JM, Van Buskirk RG, Baust JG . Addition of anticancer agents enhances freezing-induced prostate cancer cell death: implications of mitochondrial involvement. Cryobiology 2004; 49: 45–61.

    Article  CAS  PubMed  Google Scholar 

  38. Goel R, Anderson K, Slaton J, Schmidlin F, Vercellotti G, Belcher J et al. Adjuvant approaches to enhance cryosurgery. J Biomech Eng 2009; 131: 074003.

    Article  PubMed  Google Scholar 

  39. Santucci KL, Snyder KK, Baust JM, Van Buskirk RG, Mouraviev V, Polascik TJ et al. Use of 1,25alpha dihydroxyvitamin D3 as a cryosensitizing agent in a murine prostate cancer model. Prostate Cancer Prostatic Dis 2011; 14: 97–104.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Baust JG, Gage AA, Bjerklund Johansen TE, Baust JM . Mechanisms of cryoablation: clinical consequences on malignant tumors. Cryobiology 2013; 68: 1–11.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Adams JM, Cory S . The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene 2007; 26: 1324–1337.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Han B, Bischof JC . Direct cell injury associated with eutectic crystallization during freezing. Cryobiology 2004; 48: 8–21.

    Article  PubMed  Google Scholar 

  43. Han B, Iftekhar A, Bischof JC . Improved cryosurgery by use of thermophysical and inflammatory adjuvants. Technol Cancer Res Treat 2004; 3: 103–111.

    Article  PubMed  Google Scholar 

  44. Han B, Swanlund DJ, Bischof JC . Cryoinjury of MCF-7 human breast cancer cells and inhibition of post-thaw recovery using TNF-alpha. Technol Cancer Res Treat 2007; 6: 625–634.

    Article  CAS  PubMed  Google Scholar 

  45. Kimura M, Rabbani Z, Mouraviev V, Tsivian M, Caso J, Satoh T et al. Role of vitamin D3 as a sensitizer to cryoablation in a murine prostate cancer model: preliminary in vivo study. Urology 2010; 76: 764 e714–e720.

    Article  Google Scholar 

  46. Sabel MS . Cryo-immunology: a review of the literature and proposed mechanisms for stimulatory versus suppressive immune responses. Cryobiology 2009; 58: 1–11.

    Article  CAS  PubMed  Google Scholar 

  47. Berrada MS, Bischof JC . Evaluation of freezing effects on human microvascular-endothelial cells (HMEC). Cryo Lett 2001; 22: 353–366.

    CAS  Google Scholar 

  48. Hoffmann NE, Bischof JC . The cryobiology of cryosurgical injury. Urology 2002; 60: 40–49.

    Article  PubMed  Google Scholar 

  49. Hollister WR, Baust JM, Van Buskirk RG, Baust JG . Cellular components of the coronary vasculature exhibit differential sensitivity to low temperature insult. Cell Pres Technol 2003; 1: 269–280.

    Article  Google Scholar 

  50. Gilbert JC, Rubinsky B, Roos MS, Wong ST, Brennan KM . MRI-monitored cryosurgery in the rabbit brain. Magn Reson Imaging 1993; 11: 1155–1164.

    Article  CAS  PubMed  Google Scholar 

  51. Saliken JC, Donnelly BJ, Rewcastle JC . The evolution and state of modern technology for prostate cryosurgery. Urology 2002; 60: 26–33.

    Article  PubMed  Google Scholar 

  52. Baust JG, Gage AA, Clarke D, Baust JM, Van Buskirk R . Cryosurgery- a putative approach to molecular-based optimization. Cryobiology 2004; 48: 190–204.

    Article  CAS  PubMed  Google Scholar 

  53. Baust JM, Klossner DP, Robilotto A, Vanbuskirk RG, Gage AA, Mouraviev V et al. Vitamin D3 cryosensitization increases prostate cancer susceptibility to cryoablation via mitochondrial-mediated apoptosis and necrosis. BJU Int 2012; 109: 949–958.

    Article  CAS  PubMed  Google Scholar 

  54. Koushafar H, Pham L, Lee C, Rubinsky B . Chemical adjuvant cryosurgery with antifreeze proteins. J Surg Oncol 1997; 66: 114–121.

    Article  CAS  PubMed  Google Scholar 

  55. Koushafar H, Rubinsky B . Effect of antifreeze proteins on frozen primary prostatic adenocarcinoma cells. Urology 1997; 49: 421–425.

    Article  CAS  PubMed  Google Scholar 

  56. Muldrew K, Rewcastle J, Donnelly BJ, Saliken JC, Liang S, Goldie S et al. Flounder antifreeze peptides increase the efficacy of cryosurgery. Cryobiology 2001; 42: 182–189.

    Article  CAS  PubMed  Google Scholar 

  57. Pham L, Dahiya R, Rubinsky B . An in vivo study of antifreeze protein adjuvant cryosurgery. Cryobiology 1999; 38: 169–175.

    Article  CAS  PubMed  Google Scholar 

  58. Wang CL, Teo KY, Han B . An amino acidic adjuvant to augment cryoinjury of MCF-7 breast cancer cells. Cryobiology 2008; 57: 52–59.

    Article  CAS  PubMed  Google Scholar 

  59. Ikekawa S, Ishihara K, Tanaka S, Ikeda S . Basic studies of cryochemotherapy in a murine tumor system. Cryobiology 1985; 22: 477–483.

    Article  CAS  PubMed  Google Scholar 

  60. Clarke DM, Baust JM, Van Buskirk RG, Baust JG . Chemo-cryo combination therapy: an adjunctive model for the treatment of prostate cancer. Cryobiology 2001; 42: 274–285.

    Article  CAS  PubMed  Google Scholar 

  61. Clarke DM, Robilotto AT, Van Buskirk RG, Baust JG, Gage AA, Baust JM . Targeted induction of apoptosis via TRAIL and cryoablation: a novel strategy for the treatment of prostate cancer. Prostate Cancer Prostatic Dis 2007; 10: 175–184.

    Article  CAS  PubMed  Google Scholar 

  62. Forest V, Peoc'h M, Ardiet C, Campos L, Guyotat D, Vergnon JM . In vivo cryochemotherapy of a human lung cancer model. Cryobiology 2005; 51: 92–101.

    Article  CAS  PubMed  Google Scholar 

  63. Forest V, Peoc'h M, Campos L, Guyotat D, Vergnon JM . Benefit of a combined treatment of cryotherapy and chemotherapy on tumour growth and late cryo-induced angiogenesis in a non-small-cell lung cancer model. Lung Cancer 2006; 54: 79–86.

    Article  PubMed  Google Scholar 

  64. Le Pivert P, Haddad RS, Aller A, Titus K, Doulat J, Renard M et al. Ultrasound guided combined cryoablation and microencapsulated 5-fluorouracil inhibits growth of human prostate tumors in xenogenic mouse model assessed by luminescence imaging. Technol Cancer Res Treat 2004; 3: 135–142.

    Article  CAS  PubMed  Google Scholar 

  65. Mir LM, Rubinsky B . Treatment of cancer with cryochemotherapy. Br J Cancer 2002; 86: 1658–1660.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Yuan F, Zhou W, Zhang J, Zhang Z, Zou C, Huang L et al. Anticancer drugs are synergistic with freezing in induction of apoptosis in HCC cells. Cryobiology 2008; 57: 60–65.

    Article  CAS  PubMed  Google Scholar 

  67. Jiang J, Goel R, Iftekhar MA, Visaria R, Belcher JD, Vercellotti GM et al. Tumor necrosis factor-alpha-induced accentuation in cryoinjury: mechanisms in vitro and in vivo. Mol Cancer Ther 2008; 7: 2547–2555.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Goel R, Swanlund D, Coad J, Paciotti GF, Bischof JC . TNF-alpha-based accentuation in cryoinjury—dose, delivery, and response. Mol Cancer Ther 2007; 6: 2039–2047.

    Article  CAS  PubMed  Google Scholar 

  69. Shenoi MM, Iltis I, Choi J, Koonce NA, Metzger GJ, Griffin RJ et al. Nanoparticle delivered vascular disrupting agents (VDAs): use of TNF-alpha conjugated gold nanoparticles for multimodal cancer therapy. Mol Pharm 2013; 10: 1683–1694.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Udagawa M, Kudo-Saito C, Hasegawa G, Yano K, Yamamoto A, Yaguchi M 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. Clin Cancer Res 2006; 12: 7465–7475.

    Article  CAS  PubMed  Google Scholar 

  71. Gazzaniga S, Bravo A, Goldszmid SR, Maschi F, Martinelli J, Mordoh J et al. Inflammatory changes after cryosurgery-induced necrosis in human melanoma xenografted in nude mice. J Invest Dermatol 2001; 116: 664–671.

    Article  CAS  PubMed  Google Scholar 

  72. Redondo P, del Olmo J, Lopez-Diaz de Cerio A, Inoges S, Marquina M, Melero I et al. Imiquimod enhances the systemic immunity attained by local cryosurgery destruction of melanoma lesions. J Invest Dermatol 2007; 127: 1673–1680.

    Article  CAS  PubMed  Google Scholar 

  73. den Brok MH, Sutmuller RP, Nierkens S, Bennink EJ, Toonen LW, Figdor CG et al. Synergy between in situ cryoablation and TLR9 stimulation results in a highly effective in vivo dendritic cell vaccine. Cancer Res 2006; 66: 7285–7292.

    Article  CAS  PubMed  Google Scholar 

  74. den Brok MH, Nierkens S, Wagenaars JA, Ruers TJ, Schrier CC, Rijke EO et al. Saponin-based adjuvants create a highly effective anti-tumor vaccine when combined with in situ tumor destruction. Vaccine 2012; 30: 737–744.

    Article  CAS  PubMed  Google Scholar 

  75. Bassukas ID, Gamvroulia C, Zioga A, Nomikos K, Fotika C . Cryosurgery during topical imiquimod: a successful combination modality for lentigo maligna. Int J Dermatol 2008; 47: 519–521.

    Article  CAS  PubMed  Google Scholar 

  76. Waitz R, Solomon SB, Petre EN, Trumble AE, Fasso M, Norton L et al. Potent induction of tumor immunity by combining tumor cryoablation with anti-CTLA-4 therapy. Cancer Res 2012; 72: 430–439.

    Article  CAS  PubMed  Google Scholar 

  77. Chu KF, Dupuy DE . Thermal ablation of tumours: biological mechanisms and advances in therapy. Nat Rev Cancer 2014; 14: 199–208.

    Article  CAS  PubMed  Google Scholar 

  78. Tian T, Olson S, Whitacre JM, Harding A . The origins of cancer robustness and evolvability. Integr Biol (Camb) 2011; 3: 17–30.

    Article  CAS  Google Scholar 

  79. Baust JG, Klossner DP, Vanbuskirk RG, Gage AA, Mouraviev V, Polascik TJ et al. Integrin involvement in freeze resistance of androgen-insensitive prostate cancer. Prostate Cancer Prostatic Dis 2010; 13: 151–161.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Baust JM, Klossner D, Gage A, Buskirk RV, Baust JG . Akt signaling mediates prostate cancer response to cryoablation. Cryobiology 2013; 67: 427–428.

    Article  Google Scholar 

  81. Clarke DM, Robilotto AT, Rhee E, Van Buskirk RG, Baust JG, Gage AA et al. Cryoablation of renal cancer: variables involved in freezing-induced cell death. Technol Cancer Res Treat 2007; 6: 69–79.

    Article  PubMed  Google Scholar 

  82. Thompson I, Thrasher JB, Aus G, Burnett AL, Canby-Hagino ED, Cookson MS et al. Guideline for the management of clinically localized prostate cancer: 2007 update. J Urol 2007; 177: 2106–2131.

    Article  PubMed  Google Scholar 

  83. Cohen JK, Miller RJ Jr, Ahmed S, Lotz MJ, Baust J . Ten-year biochemical disease control for patients with prostate cancer treated with cryosurgery as primary therapy. Urology 2008; 71: 515–518.

    Article  PubMed  Google Scholar 

  84. Roach M III, Hanks G, Thames H Jr ., Schellhammer P, Shipley WU, Sokol GH et al. Defining biochemical failure following radiotherapy with or without hormonal therapy in men with clinically localized prostate cancer: recommendations of the RTOG-ASTRO Phoenix Consensus Conference. Int J Radiat Oncol Biol Phys 2006; 65: 965–974.

    Article  PubMed  Google Scholar 

  85. Caso JR, Tsivian M, Mouraviev V, Kimura M, Polascik TJ . Complications and postoperative events after cryosurgery for prostate cancer. BJU Int 2012; 109: 840–845.

    Article  PubMed  Google Scholar 

  86. Caso JR, Tsivian M, Mouraviev V, Polascik TJ . Predicting biopsy-proven prostate cancer recurrence following cryosurgery. Urol Oncol 2012; 30: 391–395.

    Article  PubMed  Google Scholar 

  87. Levy DA, Pisters LL, Jones JS . Primary cryoablation nadir prostate specific antigen and biochemical failure. J Urol 2009; 182: 931–937.

    Article  CAS  PubMed  Google Scholar 

  88. Pitman M, Shapiro EY, Hruby GW, Truesdale MD, Cheetham PJ, Saad S et al. Comparison of biochemical failure definitions for predicting local cancer recurrence following cryoablation of the prostate. Prostate 2012; 72: 1802–1808.

    Article  CAS  PubMed  Google Scholar 

  89. Jones JS, Rewcastle JC, Donnelly BJ, Lugnani FM, Pisters LL, Katz AE . Whole gland primary prostate cryoablation: initial results from the cryo on-line data registry. J Urol 2008; 180: 554–558.

    Article  PubMed  Google Scholar 

  90. Long JP, Bahn D, Lee F, Shinohara K, Chinn DO, Macaluso JN Jr . Five-year retrospective, multi-institutional pooled analysis of cancer-related outcomes after cryosurgical ablation of the prostate. Urology 2001; 57: 518–523.

    Article  CAS  PubMed  Google Scholar 

  91. Bahn DK, Lee F, Badalament R, Kumar A, Greski J, Chernick M . Targeted cryoablation of the prostate: 7-year outcomes in the primary treatment of prostate cancer. Urology 2002; 60: 3–11.

    Article  PubMed  Google Scholar 

  92. D'Amico AV, Moul J, Carroll PR, Sun L, Lubeck D, Chen MH . Cancer-specific mortality after surgery or radiation for patients with clinically localized prostate cancer managed during the prostate-specific antigen era. J Clin Oncol 2003; 21: 2163–2172.

    Article  PubMed  Google Scholar 

  93. Dhar N, Ward JF, Cher ML, Jones JS . Primary full-gland prostate cryoablation in older men (> age of 75 years): results from 860 patients tracked with the COLD Registry. BJU Int 2011; 108: 508–512.

    Article  PubMed  Google Scholar 

  94. Chade DC, Shariat SF, Cronin AM, Savage CJ, Karnes RJ, Blute ML et al. Salvage radical prostatectomy for radiation-recurrent prostate cancer: a multi-institutional collaboration. Eur Urol 2011; 60: 205–210.

    Article  PubMed  PubMed Central  Google Scholar 

  95. Kimura M, Mouraviev V, Tsivian M, Mayes JM, Satoh T, Polascik TJ . Current salvage methods for recurrent prostate cancer after failure of primary radiotherapy. BJU Int 2010; 105: 191–201.

    Article  CAS  PubMed  Google Scholar 

  96. Mouraviev V, Spiess PE, Jones JS . Salvage cryoablation for locally recurrent prostate cancer following primary radiotherapy. Eur Urol 2012; 61: 1204–1211.

    Article  PubMed  Google Scholar 

  97. Pisters LL, Rewcastle JC, Donnelly BJ, Lugnani FM, Katz AE, Jones JS . Salvage prostate cryoablation: initial results from the cryo on-line data registry. J Urol 2008; 180: 559–563; discussion 563–554.

    Article  PubMed  Google Scholar 

  98. Spiess PE, Given RW, Jones JS . Achieving the 'bifecta' using salvage cryotherapy for locally recurrent prostate cancer: analysis of the Cryo On-Line Data (COLD) registry data. BJU Int 2012; 110: 217–220.

    Article  PubMed  Google Scholar 

  99. Spiess PE, Levy DA, Pisters LL, Mouraviev V, Jones JS . Outcomes of salvage prostate cryotherapy stratified by pre-treatment PSA: update from the COLD registry. World J Urol 2013; 31: 1321–1325.

    Article  CAS  PubMed  Google Scholar 

  100. Williams AK, Martinez CH, Lu C, Ng CK, Pautler SE, Chin JL . Disease-free survival following salvage cryotherapy for biopsy-proven radio-recurrent prostate cancer. Eur Urol 2011; 60: 405–410.

    Article  PubMed  Google Scholar 

  101. Wenske S, Quarrier S, Katz AE . Salvage cryosurgery of the prostate for failure after primary radiotherapy or cryosurgery: long-term clinical, functional, and oncologic outcomes in a large cohort at a tertiary referral centre. Eur Urol 2013; 64: 1–7.

    Article  PubMed  Google Scholar 

  102. Aron M, Kamoi K, Remer E, Berger A, Desai M, Gill I . Laparoscopic renal cryoablation: 8-year, single surgeon outcomes. J Urol 2010; 183: 889–895.

    Article  PubMed  Google Scholar 

  103. Lusch A, Bucur P, Okhunov Z, Kavoussi L, Badani K, Derweesh I et al. Intermediate term oncologic outcomes of renal cryoablation: an international multi-institutional analysis (submitted) 2014.

Download references

Acknowledgements

This report was supported in part from funding from the NIH and CPSI Biotech. We thank Ms Sara E Palmer for her diligent efforts in the preparation of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J G Baust.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Baust, J., Bischof, J., Jiang-Hughes, S. et al. Re-purposing cryoablation: a combinatorial ‘therapy’ for the destruction of tissue. Prostate Cancer Prostatic Dis 18, 87–95 (2015). https://doi.org/10.1038/pcan.2014.54

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/pcan.2014.54

This article is cited by

Search

Quick links