Models and Mechanisms of Tissue Injury in Cryosurgery
Anthony T. Robilotto
Institute of Biomedical Technology, State University of New York at Binghamton, Binghamton, NY, USA
Department of Biological Sciences, Binghamton University, Binghamton, NY, USA
CPSI Biotech, Owego, NY, USA
Search for more papers by this authorJohn M. Baust
Institute of Biomedical Technology, State University of New York at Binghamton, Binghamton, NY, USA
CPSI Biotech, Owego, NY, USA
Search for more papers by this authorRobert G. Van Buskirk
Institute of Biomedical Technology, State University of New York at Binghamton, Binghamton, NY, USA
Department of Biological Sciences, Binghamton University, Binghamton, NY, USA
CPSI Biotech, Owego, NY, USA
Search for more papers by this authorJohn G. Baust
Institute of Biomedical Technology, State University of New York at Binghamton, Binghamton, NY, USA
Department of Biological Sciences, Binghamton University, Binghamton, NY, USA
Search for more papers by this authorAnthony T. Robilotto
Institute of Biomedical Technology, State University of New York at Binghamton, Binghamton, NY, USA
Department of Biological Sciences, Binghamton University, Binghamton, NY, USA
CPSI Biotech, Owego, NY, USA
Search for more papers by this authorJohn M. Baust
Institute of Biomedical Technology, State University of New York at Binghamton, Binghamton, NY, USA
CPSI Biotech, Owego, NY, USA
Search for more papers by this authorRobert G. Van Buskirk
Institute of Biomedical Technology, State University of New York at Binghamton, Binghamton, NY, USA
Department of Biological Sciences, Binghamton University, Binghamton, NY, USA
CPSI Biotech, Owego, NY, USA
Search for more papers by this authorJohn G. Baust
Institute of Biomedical Technology, State University of New York at Binghamton, Binghamton, NY, USA
Department of Biological Sciences, Binghamton University, Binghamton, NY, USA
Search for more papers by this authorDevashish Shrivastava
US Food and Drug Administration, Silver Spring, NY, 10903 USA
Search for more papers by this authorSummary
Cryotherapies are used for the management of pain and inflammation, the ablation of neoplastic lesions, and the removal of diseased or damaged tissues. This chapter discusses types of injuries: hypothermic injury, freezing injury, thawing injury, and post-thaw injury. A number of culture models are available for the study of cryosurgical procedures and cellular responses to low temperatures, including acellular hydrogels, monolayer cultures, animal models, tissue-engineered constructs, and clinical studies. The identification of biochemical and immunological cell death in the periphery of the cryolesion has afforded the opportunity to attenuate the freeze margin through the use of adjuvants or adjunctive therapies. Advances in cryosurgical technologies are aiming to make cryosurgery colder, faster, and more destructive, potentially expanding its application to even more diverse tissues and disease states. Studies into the phenomenon of cryoimmunity hold tremendous value as the possibility of systemic benefit from localized treatments could drastically alter cancer treatments.
References
- Cooper, S.M. and R.P. Dawber, The history of cryosurgery. J R Soc Med, 2001. 94(4): pp. 196–201.
-
Korpan, N.N., A history of cryosurgery: Its development and future. J Am Coll Surg, 2007. 204(2): pp. 314–324.
10.1016/j.jamcollsurg.2006.11.006 Google Scholar
- Cooper, I.S. and A.S. Lee, Cryostatic congelation: A system for producing a limited, controlled region of cooling or freezing of biologic tissues. J Nerv Ment Dis, 1961. 133: pp. 259–263.
- Kuflik, E.G., et al., Millennium paper: History of dermatologic cryosurgery. Dermatol Surg, 2000. 26(8): pp. 715–722.
- Hachisuka, J., K. Doi, and M. Furue, Combination cryosurgery with hyperthermia in the management of skin metastasis from breast cancer: A case report. Int J Surg Case Rep, 2012. 3(2): pp. 68–69.
-
Bassukas, I.D. and G. Gaitanis, Combination of cryosurgery and topical imiquimod: Does timing matter for successful immunocryosurgery? Cryobiology, 2009. 59(1): pp. 116–117.
10.1016/j.cryobiol.2009.04.011 Google Scholar
- Farhangian, M.E., et al., Cutaneous cryosurgery in the United States. J Dermatolog Treat, 2016. 27(1): pp. 91–94.
- Thai, K.E. and R.D. Sinclair, Cryosurgery of benign skin lesions. Australas J Dermatol, 1999. 40(4): pp. 175–184; quiz 185–186.
- Reuter, H.J., Endoscopic cryosurgery of prostate and bladder tumors. J Urol, 1972. 107(3): pp. 389–393.
- Goikhberg, M.I., et al., Cryosurgical treatment of bladder cancer. Urol Nefrol (Mosk), 1979( 2): pp. 24–27.
- Li, Z., et al., Cryoablation plus chemotherapy in colorectal cancer patients with liver metastases. Tumour Biol, 2014. 35(11): pp. 10841–10848.
-
Mala, T., et al., Cryoablation of colorectal liver metastases: Minimally invasive tumour control. Scand J Gastroenterol, 2004. 39(6): pp. 571–578.
10.1080/00365520410000510 Google Scholar
- Muti, R. and G. Filogamo, Extrinsic denervation of the intestine by using a cryogenic probe. Minerva Med, 1974. 65(70): pp. 3649–3650.
- Scholvinck, D.W., et al., Treatment of Barrett's esophagus with a novel focal cryoablation device: A safety and feasibility study. Endoscopy, 2015. 47(12): pp. 1106–1112.
-
Polascik, T.J., J.M. Mayes, and V. Mouraviev, Nerve-sparing focal cryoablation of prostate cancer. Curr Opin Urol, 2009. 19(2): pp. 182–187.
10.1097/MOU.0b013e328323f603 Google Scholar
- Onik, G., et al., The “male lumpectomy”: Focal therapy for prostate cancer using cryoablation results in 48 patients with at least 2-year follow-up. Urol Oncol, 2008. 26(5): pp. 500–505.
- Marshall, A., Cryogenic surgery of the prostate. Proc R Soc Med, 1968. 61(11 Part 1): pp. 1139–1142.
- Grossgold, E., et al., Does neoadjuvant androgen deprivation therapy before primary whole gland cryoablation of the prostate affect the outcome? Urology, 2014. 83(2): pp. 379–383.
-
Rand, R.W., et al., Cryolumpectomy for breast cancer: An experimental study. Cryobiology, 1985. 22(4): pp. 307–318.
10.1016/0011-2240(85)90178-6 Google Scholar
-
Bland, K.L., J. Gass, and V.S. Klimberg, Radiofrequency, cryoablation, and other modalities for breast cancer ablation. Surg Clin North Am, 2007. 87(2): pp. 539–550, xii.
10.1016/j.suc.2007.02.003 Google Scholar
- Sabel, M.S., Cryoablation for breast cancer: No need to turn a cold shoulder. J Surg Oncol, 2008. 97(6): pp. 485–486.
- Davol, P.E., B.R. Fulmer, and D.B. Rukstalis, Long-term results of cryoablation for renal cancer and complex renal masses. Urology, 2006. 68(suppl. 1): pp. 2–6.
- Rodriguez Faba, O., et al., Kidney cancer focal cryoablation trend: Does location or approach matter? World J Urol, 2015.
- Niu, L.Z., J.L. Li, and K.C. Xu, Percutaneous cryoablation for liver cancer. J Clin Transl Hepatol, 2014. 2(3): pp. 182–188.
-
Hinshaw, J.L. and F.T. Lee, Jr. Cryoablation for liver cancer. Tech Vasc Interv Radiol, 2007. 10(1): pp. 47–57.
10.1053/j.tvir.2007.08.005 Google Scholar
-
Gage, A.M., M. Montes, and A.A. Gage, Destruction of hepatic and splenic tissue by freezing and heating. Cryobiology, 1982. 19(2): pp. 172–179.
10.1016/0011-2240(82)90138-9 Google Scholar
- Callstrom, M.R., et al., Percutaneous image-guided cryoablation of painful metastases involving bone: Multicenter trial. Cancer, 2013. 119(5): pp. 1033–1041.
- Regling, G., Cryogenic surgery for orthopedics. Possibilities of destruction through cold in bone tumors which are difficult to treat. Beitr Orthop Traumatol, 1974. 21(12): pp. 716–724.
- Gage, A.A., et al., Freezing bone without excision. An experimental study of bone-cell destruction and manner of regrowth in dogs. JAMA, 1966. 196(9): pp. 770–774.
- Cooper, I.S. and S. Stellar, Cryogenic freezing of brain tumors for excision or destruction in situ. J Neurosurg, 1963. 20: pp. 921–930.
- Ba, Y.F., et al., Comparison of the analgesic effects of cryoanalgesia vs. parecoxib for lung cancer patients after lobectomy. Surg Today, 2015. 45(10): pp. 1250–1254.
- Schmidt, K.L., et al., Heat, cold and inflammation. Z Rheumatol, 1979. 38(11–12): pp. 391–404.
- Kimman, G.J., et al., One-year follow-up in a prospective, randomized study comparing radiofrequency and cryoablation of arrhythmias in Koch's triangle: Clinical symptoms and event recording. Europace, 2006. 8(8): pp. 592–595.
- Friedman, P.L., Catheter cryoablation of cardiac arrhythmias. Curr Opin Cardiol, 2005. 20(1): pp. 48–54.
- Skanes, A.C., et al., Cryoablation of atrial arrhythmias. Card Electrophysiol Rev, 2002. 6(4): pp. 383–388.
-
Bingler, M.A., J.R. Darst, and T.E. Fagan, Cryo-balloon angioplasty for pulmonary vein stenosis in pediatric patients. Pediatr Cardiol, 2012. 33(1): pp. 109–114.
10.1007/s00246-011-0099-1 Google Scholar
- Tse, H.F., et al., Pulmonary vein isolation using transvenous catheter cryoablation for treatment of atrial fibrillation without risk of pulmonary vein stenosis. J Am Coll Cardiol, 2003. 42(4): pp. 752–758.
-
Baust, J.G. and A.A. Gage, Progress toward optimization of cryosurgery. Technol Cancer Res Treat, 2004. 3(2): pp. 95–101.
10.1177/153303460400300202 Google Scholar
- Lovelock, J.E., Biophysical aspects of the freezing and thawing of living cells. Proc R Soc Med, 1954. 47(1): pp. 60–62.
- Pitt, R.E. and P.L. Steponkus, Quantitative analysis of the probability of intracellular ice formation during freezing of isolated protoplasts. Cryobiology, 1989. 26(1): pp. 44–63.
- Mazur, P., Cryobiology: The freezing of biological systems. Science, 1970. 168(3934): pp. 939–949.
- Mazur, P., Kinetics of water loss from cells at subzero temperatures and the likelihood of intracellular freezing. J Gen Physiol, 1963. 47: pp. 347–369.
- Baust, J.M., et al., A molecular basis of cryopreservation failure and its modulation to improve cell survival. Cell Transplant, 2001. 10(7): pp. 561–571.
- Gage, A.A. and J. Baust, Mechanisms of tissue injury in cryosurgery. Cryobiology, 1998. 37(3): pp. 171–186.
- Baust, J.G., et al., Mechanisms of cryoablation: Clinical consequences on malignant tumors. Cryobiology, 2014. 68(1): pp. 1–11.
-
Litvan, G.G., Mechanism of cryoinjury in biological systems. Cryobiology, 1972. 9(3): pp. 182–191.
10.1016/0011-2240(72)90030-2 Google Scholar
- Baust, J.G., D. Gao, and J.M. Baust, Cryopreservation: An emerging paradigm change. Organogenesis, 2009. 5(3): pp. 90–96.
- Yiu, W.K., et al., Cryosurgery: A review. Int J Angiol, 2007. 16(1): pp. 1–6.
- Brinkley, B.R. and J. Cartwright, Jr. Cold-labile and cold-stable microtubules in the mitotic spindle of mammalian cells. Ann N Y Acad Sci, 1975. 253: pp. 428–439.
- Zenzes, M.T., et al., Effects of chilling to 0 degrees C on the morphology of meiotic spindles in human metaphase II oocytes. Fertil Steril, 2001. 75(4): pp. 769–777.
- Stefanovich, P., et al., Effects of hypothermia on the function, membrane integrity, and cytoskeletal structure of hepatocytes. Cryobiology, 1995. 32(4): pp. 389–403.
- Baust, J.G. and A.A. Gage, The molecular basis of cryosurgery. BJU Int, 2005. 95(9): pp. 1187–1191.
- Muldrew, K. and L.E. McGann, Mechanisms of intracellular ice formation. Biophys J, 1990. 57(3): pp. 525–532.
- Wesley-Smith, J., et al., Why is intracellular ice lethal? A microscopical study showing evidence of programmed cell death in cryo-exposed embryonic axes of recalcitrant seeds of Acer saccharinum. Ann Bot, 2015. 115(6): pp. 991–1000.
- Pegg, D.E., Mechanisms of freezing damage. Symp Soc Exp Biol, 1987. 41: pp. 363–378.
- Meryman, H.T., Mechanics of freezing in living cells and tissues. Science, 1956. 124(3221): pp. 515–521.
- Sherman, J.K., Survival of higher animal cells after the formation and dissolution of intracellular ice. Anat Rec, 1962. 144: pp. 171–189.
- Mazur, P., The role of intracellular freezing in the death of cells cooled at supraoptimal rates. Cryobiology, 1977. 14(3): pp. 251–272.
- Mazur, P., S.P. Leibo, and E.H. Chu, A two-factor hypothesis of freezing injury. Evidence from Chinese hamster tissue-culture cells. Exp Cell Res, 1972. 71(2): pp. 345–355.
- Baust, J., et al., Minimally invasive cryosurgery: Technological advances. Cryobiology, 1997. 34(4): pp. 373–384.
- Yang, G., A. Zhang, and L.X. Xu, Intracellular ice formation and growth in MCF-7 cancer cells. Cryobiology, 2011. 63(1): pp. 38–45.
- Steponkus, P.L. and D.V. Lynch, Freeze/thaw-induced destabilization of the plasma membrane and the effects of cold acclimation. J Bioenerg Biomembr, 1989. 21(1): pp. 21–41.
- Meryman, H.T., Modified model for the mechanism of freezing injury in erythrocytes. Nature, 1968. 218(5139): pp. 333–336.
-
Washington, K., et al., Hepatic cryoablation-induced acute lung injury: Histopathologic findings. J Surg Res, 2001. 95(1): pp. 1–7.
10.1006/jsre.2000.5976 Google Scholar
- Sindelar, W.F., N. Javadpour, and D.H. Bagley, Histological and ultrastructural changes in rat kidney after cryosurgery. J Surg Oncol, 1981. 18(4): pp. 363–379.
- Marzella, L., et al., Morphologic characterization of acute injury to vascular endothelium of skin after frostbite. Plast Reconstr Surg, 1989. 83(1): pp. 67–76.
- Gage, A.A., J.M. Baust, and J.G. Baust, Experimental cryosurgery investigations in vivo. Cryobiology, 2009. 59(3): pp. 229–243.
-
Cino, M. and R.F. Del Maestro, Generation of hydrogen peroxide by brain mitochondria: The effect of reoxygenation following postdecapitative ischemia. Arch Biochem Biophys, 1989. 269(2): pp. 623–638.
10.1016/0003-9861(89)90148-3 Google Scholar
- Hamberg, M., J. Svensson, and B. Samuelsson, Thromboxanes: A new group of biologically active compounds derived from prostaglandin endoperoxides. Proc Natl Acad Sci USA, 1975. 72(8): pp. 2994–2998.
- White, B.C., J.G. Wiegenstein, and C.D. Winegar, Brain ischemic anoxia. Mechanisms of injury. JAMA, 1984. 251(12): pp. 1586–1590.
- Wang, R., et al., Three-dimensional co-culture models to study prostate cancer growth, progression, and metastasis to bone. Semin Cancer Biol, 2005. 15(5): pp. 353–364.
-
Griffin, R.J., et al., Assessing pH and oxygenation in cryotherapy-induced cytotoxicity and tissue response to freezing. Technol Cancer Res Treat, 2004. 3(3): pp. 245–251.
10.1177/153303460400300302 Google Scholar
- Isoda, H., et al., Gel phantom study of a cryosurgical probe with a thermosiphon effect and liquid nitrogen-cooled aluminum thermal storage blocks. Nagoya J Med Sci, 2015. 77(3): pp. 399–407.
- Shaikh, A.M., A. Srivastava, and M.D. Atrey, Next generation design, development, and evaluation of cryoprobes for minimally invasive surgery and solid cancer therapeutics: In silico and computational studies. OMICS, 2015. 19(2): pp. 131–144.
-
Etheridge, M.L., et al., Methods for characterizing convective cryoprobe heat transfer in ultrasound gel phantoms. J Biomech Eng, 2013. 135(2): pp. 021002.
10.1115/1.4023237 Google Scholar
- Birkenmaier, C., et al., The gel box: A testing device for the characterization of cryo- and radiofrequency lesions employed in interventional pain therapy. Pain Physician, 2010. 13(3): pp. 263–271.
-
Rabin, Y., Key issues in bioheat transfer simulations for the application of cryosurgery planning. Cryobiology, 2008. 56(3): pp. 248–250.
10.1016/j.cryobiol.2008.02.004 Google Scholar
- Antoni, D., et al., Three-dimensional cell culture: A breakthrough in vivo. Int J Mol Sci, 2015. 16(3): pp. 5517–5527.
- Clarke, D.M., et al., Cryoablation of renal cancer: Variables involved in freezing-induced cell death. Technol Cancer Res Treat, 2007. 6(2): pp. 69–79.
- Hollister, W.R., Mathew, A. J., Baust, et al., The effects of freezing on cell viability and mechanisms of cell death in an in vitro human prostate cancer cell line. Molecular Urology, 1998. 2: pp. 13–19.
- Clarke, D.M., et al., Chemo-cryo combination therapy: An adjunctive model for the treatment of prostate cancer. Cryobiology, 2001. 42(4): pp. 274–285.
- Clarke, D.M., et al., Cryosurgical modeling: Sequence of freezing and cytotoxic agent application affects cell death. Mol Urol, 1999. 3(1): pp. 25–31.
- Clarke, D.M., et al., Targeted induction of apoptosis via TRAIL and cryoablation: A novel strategy for the treatment of prostate cancer. Prostate Cancer Prostatic Dis, 2007. 10(2): pp. 175–184.
-
Robilotto, A.T., et al., Development of a tissue engineered human prostate tumor equivalent for use in the evaluation of cryoablative techniques. Technol Cancer Res Treat, 2007. 6(2): pp. 81–89.
10.1177/153303460700600204 Google Scholar
- Robilotto, A.T., et al., Temperature-dependent activation of differential apoptotic pathways during cryoablation in a human prostate cancer model. Prostate Cancer Prostatic Dis, 2013. 16(1): pp. 41–49.
- Hanai, A., W.L. Yang, and T.S. Ravikumar, Induction of apoptosis in human colon carcinoma cells HT29 by sublethal cryo-injury: Mediation by cytochrome c release. Int J Cancer, 2001. 93(4): pp. 526–533.
- Yang, W.L., et al., Apoptosis induced by cryo-injury in human colorectal cancer cells is associated with mitochondrial dysfunction. Int J Cancer, 2003. 103(3): pp. 360–369.
- Clarke, D.M., et al., Addition of anticancer agents enhances freezing-induced prostate cancer cell death: Implications of mitochondrial involvement. Cryobiology, 2004. 49(1): pp. 45–61.
- Baust, J.M., et al., Vitamin D(3) cryosensitization increases prostate cancer susceptibility to cryoablation via mitochondrial-mediated apoptosis and necrosis. BJU Int, 2012. 109(6): pp. 949–958.
-
Stott, S.L. and J.O. Karlsson, Visualization of intracellular ice formation using high-speed video cryomicroscopy. Cryobiology, 2009. 58(1): pp. 84–95.
10.1016/j.cryobiol.2008.11.003 Google Scholar
- Mazur, P., Freezing of living cells: Mechanisms and implications. Am J Physiol, 1984. 247(3 Pt 1): pp. C125–C142.
- Hutchinson, L. and R. Kirk, High drug attrition rates: Where are we going wrong? Nat Rev Clin Oncol, 2011. 8(4): pp. 189–190.
- Cahan, W.G. and A.F. Montesa-Cruz, Cryotonsillectomy in dogs. Arch Otolaryngol, 1965. 81: pp. 372–378.
-
Guiraudon, G.M., et al., En bloc exclusion of the pulmonary vein region in the pig using off pump, beating, intra-cardiac surgery: A pilot study of minimally invasive surgery for atrial fibrillation. Ann Thorac Surg, 2005. 80(4): pp. 1417–1423.
10.1016/j.athoracsur.2005.03.047 Google Scholar
-
Smith, J.J. and J. Fraser, An estimation of tissue damage and thermal history in the cryolesion. Cryobiology, 1974. 11(2): pp. 139–147.
10.1016/0011-2240(74)90303-4 Google Scholar
-
Gage, A.A., Experimental cryogenic injury of the palate: Observations pertinent to cryosurgical destruction of tumors. Cryobiology, 1978. 15(4): pp. 415–425.
10.1016/0011-2240(78)90060-3 Google Scholar
-
Yiu, W.K., S.W. Cheng, and B.E. Sumpio, Synergistic effect of cool/thaw cycles on vascular cells in an in vitro model of cryoplasty. J Vasc Interv Radiol, 2008. 19(6): pp. 925–930.
10.1016/j.jvir.2008.02.007 Google Scholar
- Nishida, H., et al., Cryoimmunology for malignant bone and soft-tissue tumors. Int J Clin Oncol, 2011. 16(2): pp. 109–117.
- Machlenkin, A., et al., Combined dendritic cell cryotherapy of tumor induces systemic antimetastatic immunity. Clin Cancer Res, 2005. 11(13): pp. 4955–4961.
- Kawamura, N., et al., Intratumoral injection of BCG-CWS-pretreated dendritic cells following tumor cryoablation. Methods Mol Biol, 2014. 1139: pp. 145–153.
- Urano, M., et al., 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, 2003. 46(3): pp. 238–245.
- Forest, V., et al., Optimisation and molecular signalling of apoptosis in sequential cryotherapy and chemotherapy combination in human A549 lung cancer xenografts in SCID mice. Br J Cancer, 2009. 100(12): pp. 1896–1902.
- Ikekawa, S., et al., Basic studies of cryochemotherapy in a murine tumor system. Cryobiology, 1985. 22(5): pp. 477–483.
- Goel, R., et al., TNF-alpha-based accentuation in cryoinjury: Dose, delivery, and response. Mol Cancer Ther, 2007. 6(7): pp. 2039–2047.
- Kimura, M., et al., Role of vitamin D(3) as a sensitizer to cryoablation in a murine prostate cancer model: Preliminary in vivo study. Urology, 2010. 76(3): pp. 764, e14–e20.
- Mak, I.W., N. Evaniew, and M. Ghert, Lost in translation: Animal models and clinical trials in cancer treatment. Am J Transl Res, 2014. 6(2): pp. 114–118.
-
Han, B., et al., A cryoinjury model using engineered tissue equivalents for cryosurgical applications. Ann Biomed Eng, 2005. 33(7): pp. 972–982.
10.1007/s10439-005-3478-z Google Scholar
- Xu, X., M.C. Farach-Carson, and X. Jia, Three-dimensional in vitro tumor models for cancer research and drug evaluation. Biotechnol Adv, 2014. 32(7): pp. 1256–1268.
-
Homasson, J.P., et al., Tumor fixation of bleomycin labeled with 57 cobalt before and after cryotherapy of bronchial carcinoma. Cryobiology, 1992. 29(5): pp. 543–548.
10.1016/0011-2240(92)90059-B Google Scholar
- Hoover, W.D., 3rd et al., Efficacy of cryosurgery and 5-fluorouracil cream 0.5% combination therapy for the treatment of actinic keratosis. Cutis, 2014. 94(5): pp. 255–259.
- Yuanying, Y., et al., Therapeutic outcomes of combining cryotherapy, chemotherapy and DC-CIK immunotherapy in the treatment of metastatic non-small cell lung cancer. Cryobiology, 2013. 67(2): pp. 235–240.
- Gu, X.Y., Z. Jiang, and W. Fang, Cryoablation combined with molecular target therapy improves the curative effect in patients with advanced non-small cell lung cancer. J Int Med Res, 2011. 39(5): pp. 1736–1743.
- Thakur, A., et al., 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. J Immunother, 2011. 34(5): pp. 457–467.
- Si, T., Z. Guo, and X. Hao, Combined cryoablation and GM-CSF treatment for metastatic hormone refractory prostate cancer. J Immunother, 2009. 32(1): pp. 86–91.
- Redondo, P., et al., Imiquimod enhances the systemic immunity attained by local cryosurgery destruction of melanoma lesions. J Invest Dermatol, 2007. 127(7): pp. 1673–1680.
-
Smith, J.J., J. Fraser, and A.G. MacIver, Ultrastructure after cryosurgery of rat liver. Cryobiology, 1978. 15(4): pp. 426–432.
10.1016/0011-2240(78)90061-5 Google Scholar
- Zouboulis, C.C., Principles of cutaneous cryosurgery: An update. Dermatology, 1999. 198(2): pp. 111–117.
- Klossner, D.P., et al., Cryosurgical technique: Assessment of the fundamental variables using human prostate cancer model systems. Cryobiology, 2007. 55(3): pp. 189–199.
- Andrews, M.D., Cryosurgery for common skin conditions. Am Fam Physician, 2004. 69(10): pp. 2365–2372.
- Zimmerman, E.E. and P. Crawford, Cutaneous cryosurgery. Am Fam Physician, 2012. 86(12): pp. 1118–1124.
- Li, R., et al., The effect of androgen deprivation therapy before salvage whole-gland cryoablation after primary radiation failure in prostate cancer treatment. Urology, 2015. 85(5): pp. 1137–1142.
- Klossner, D.P., et al., Cryoablative response of prostate cancer cells is influenced by androgen receptor expression. BJU Int, 2008. 101(10): pp. 1310–1316.
-
Baust, J.G., et al., Integrin involvement in freeze resistance of androgen-insensitive prostate cancer. Prostate Cancer Prostatic Dis, 2010. 13(2): pp. 151–161.
10.1038/pcan.2009.59 Google Scholar
- Farrant, J. and C.A. Walter, The cryobiological basis for cryosurgery. J Dermatol Surg Oncol, 1977. 3(4): pp. 403–407.
- Pazhayannur, P.V. and J.C. Bischof, Measurement and simulation of water transport during freezing in mammalian liver tissue. J Biomech Eng, 1997. 119(3): pp. 269–277.
- Bischof, J.C., et al., Cryosurgery of dunning AT-1 rat prostate tumor: Thermal, biophysical, and viability response at the cellular and tissue level. Cryobiology, 1997. 34(1): pp. 42–69.
- Bischof, J., K. Christov, and B. Rubinsky, A morphological study of cooling rate response in normal and neoplastic human liver tissue: Cryosurgical implications. Cryobiology, 1993. 30(5): pp. 482–492.
- Hong, J.S. and B. Rubinsky, Patterns of ice formation in normal and malignant breast tissue. Cryobiology, 1994. 31(2): pp. 109–120.
-
Rui, J., et al., Effect of thermal variables on human breast cancer in cryosurgery. Breast Cancer Res Treat, 1999. 53(2): pp. 185–192.
10.1023/A:1006182618414 Google Scholar
- Woolley, M.L., et al., Effect of freezing parameters (freeze cycle and thaw process) on tissue destruction following renal cryoablation. J Endourol, 2002. 16(7): pp. 519–522.
- Stewart, G.J., et al., Hepatic cryotherapy: Double-freeze cycles achieve greater hepatocellular injury in man. Cryobiology, 1995. 32(3): pp. 215–219.
- Schantz, A. and L. Thormann, Cryosurgery for dysplasia of the uterine ectocervix: A randomized study of the efficacy of the single- and double-freeze techniques. Acta Obstet Gynecol Scand, 1984. 63(5): pp. 417–420.
- Znati, C.A., et al., Variables influencing response of human prostate carcinoma cells to combined radiation and cryotherapy in vitro . Cryobiology, 1998. 37: pp. 376–452.
- Hollister, W.R., et al., Effects of freezing of cell viability and mechanisms of cell death in a human prostate cell line. Mol Urol, 1998. 2: pp. 3–18.
- Gage, A.A., et al., Effect of varying freezing and thawing rates in experimental cryosurgery. Cryobiology, 1985. 22(2): pp. 175–182.
-
Neel, H.B., 3rd, A.S. Ketcham, and W.G. Hammond, Cryonecrosis of normal and tumor-bearing rat liver potentiated by inflow occlusion. Cancer, 1971. 28(5): pp. 1211–1218.
10.1002/1097-0142(1971)28:5<1211::AID-CNCR2820280519>3.0.CO;2-C PubMed Web of Science® Google Scholar
- Whittaker, D.K., Mechanisms of tissue destruction following cryosurgery. Ann R Coll Surg Engl, 1984. 66(5): pp. 313–318.
- Cahan, W.G., Cryosurgery of malignant and benign tumors. Fed Proc, 1965. 24: pp. S241–S248.
- Cooper, I.S., Cryogenic surgery for cancer. Fed Proc, 1965. 24: pp. S237–S240.
-
Gage, A.A., et al., Cryotherapy for cancer of the lip and oral cavity. Cancer, 1965. 18(12): pp. 1646–1651.
10.1002/1097-0142(196512)18:12<1646::AID-CNCR2820181221>3.0.CO;2-Y PubMed Web of Science® Google Scholar
- Mallon, E. and R. Dawber, Cryosurgery in the treatment of basal cell carcinoma: Assessment of one and two freeze-thaw cycle schedules. Dermatol Surg, 1996. 22(10): pp. 854–858.
- Hinshaw, J.L., et al., Optimizing the protocol for pulmonary cryoablation: A comparison of a dual- and triple-freeze protocol. Cardiovasc Intervent Radiol, 2010. 33(6): pp. 1180–1185.
- Tse, H.F., et al., Effects of temporal application parameters on lesion dimensions during transvenous catheter cryoablation. J Cardiovasc Electrophysiol, 2005. 16(2): pp. 201–204.
- Whittaker, D.K., Observations on ice crystals in tissue subjected to repeat freezing. Proc R Soc Med, 1975. 68(10): pp. 603–605.
-
Jaworska, D., W. Krol, and E. Szliszka, Prostate cancer stem cells: Research advances. Int J Mol Sci, 2015. 16(11): pp. 27433–27449.
10.3390/ijms161126036 Google Scholar
- Soussi, T., p53 alterations in human cancer: More questions than answers. Oncogene, 2007. 26(15): pp. 2145–2156.
- Elmore, S., Apoptosis: A review of programmed cell death. Toxicol Pathol, 2007. 35(4): pp. 495–516.
- Leibovici, D., et al., Ultrashort intracorporeally maneuverable cryoprobes for laparoscopic renal cryoablation in the porcine model. Surg Endosc, 2008. 22(6): pp. 1519–1524.
- Korpan, N.N., Cryosurgery: Early ultrastructural changes in liver tissue in vivo. J Surg Res, 2009. 153(1): pp. 54–65.
- Li, M., et al., Argon-helium cryosurgery for treatment of C6 gliomas in rats and its effect on cellular immunity. Technol Cancer Res Treat, 2010. 9(1): pp. 87–94.
- Liu, J.G., et al., Cryosurgery for treatment of subcutaneously xenotransplanted tumors in rats and its effect on cellular immunity. Technol Cancer Res Treat, 2011. 10(4): pp. 339–346.
- Kimura, M., et al., Morphology of hypoxia following cryoablation in a prostate cancer murine model: Its relationship to necrosis, apoptosis and, microvessel density. Cryobiology, 2010. 61(1): pp. 148–154.
- Wen, J., et al., Cryoablation induces necrosis and apoptosis in lung adenocarcinoma in mice. Technol Cancer Res Treat, 2007. 6(6): pp. 635–640.
-
Liu, T., et al., Extracts from glioma tissues following cryoablation have proapoptosis, antiproliferation, and anti-invasion effects on glioma cells. Biomed Res Int, 2014. 2014: pp. 236939.
10.1155/2014/236939 Google Scholar
-
Grdovic, N., et al., Proteolytic events in cryonecrotic cell death: Proteolytic activation of endonuclease P23. Cryobiology, 2010. 60(3): pp. 271–280.
10.1016/j.cryobiol.2010.01.005 Google Scholar
- Steinbach, J.P., J. Weissenberger, and A. Aguzzi, Distinct phases of cryogenic tissue damage in the cerebral cortex of wild-type and c-fos deficient mice. Neuropathol Appl Neurobiol, 1999. 25(6): pp. 468–480.
- Zhang, D., et al., ROS-induced oxidative stress and apoptosis-like event directly affect the cell viability of cryopreserved embryogenic callus in Agapanthus praecox. Plant Cell Rep, 2015. 34(9): pp. 1499–1513.
- Corwin, W.L., et al., Characterization and modulation of human mesenchymal stem cell stress pathway response following hypothermic storage. Cryobiology, 2014. 68(2): pp. 215–226.
- Wagh, V., et al., Effects of cryopreservation on the transcriptome of human embryonic stem cells after thawing and culturing. Stem Cell Rev, 2011. 7(3): pp. 506–517.
- Sabel, M.S., Cryo-immunology: A review of the literature and proposed mechanisms for stimulatory versus suppressive immune responses. Cryobiology, 2009. 58(1): pp. 1–11.
- Sidana, A., et al., Cryoimmunotherapy in urologic oncology. Urology, 2010. 75(5): pp. 1009–1014.
- Shulman, S., C. Yantorno, and P. Bronson, Cryo-immunology: A method of immunization to autologous tissue. Proc Soc Exp Biol Med, 1967. 124(2): pp. 658–661.
- Ablin, R.J., Cryoimmunotherapy. Br Med J, 1972. 3(5824): pp. 476.
- Soanes, W.A., R.J. Ablin, and M.J. Gonder, Remission of metastatic lesions following cryosurgery in prostatic cancer: Immunologic considerations. J Urol, 1970. 104(1): pp. 154–159.
- Tanaka, S., Immunological aspects of cryosurgery in general surgery. Cryobiology, 1982. 19(3): pp. 247–262.
- Blackwood, C.E. and I.S. Cooper, Response of experimental tumor systems to cryosurgery. Cryobiology, 1972. 9(6): pp. 508–515.
- Bagley, D.H., et al., Lymphocyte mediated cytotoxicity after cryosurgery of a murine sarcoma. J Surg Res, 1974. 17(6): pp. 404–406.
- Lubaroff, D.M., et al., Immunologic aspects of the prostate. Prostate, 1981. 2(3): pp. 233–248.
-
Joosten, J.J., et al.,
In vivo destruction of tumor tissue by cryoablation can induce inhibition of secondary tumor growth: An experimental study. Cryobiology, 2001. 42(1): pp. 49–58.
10.1006/cryo.2001.2302 Google Scholar
-
Sabel, M.S., et al., Immunologic response to cryoablation of breast cancer. Breast Cancer Res Treat, 2005. 90(1): pp. 97–104.
10.1007/s10549-004-3289-1 Google Scholar
-
Allen, P.J., et al., The effects of hepatic cryosurgery on tumor growth in the liver. J Surg Res, 1998. 77(2): pp. 132–136.
10.1006/jsre.1998.5365 Google Scholar
- Zonnevylle, J.A. and A. Zwaveling, The influence of cryosurgery and electrocoagulation upon metastatic spread. J Surg Oncol, 1984. 27(2): pp. 131–134.
- Yamashita, T., et al., Enhanced tumor metastases in rats following cryosurgery of primary tumor. Gan, 1982. 73(2): pp. 222–228.
-
Friedman, E.J., et al., Cryosurgical ablation of the normal ventral prostate plus adjuvant does not protect Copenhagen rats from Dunning prostatic adenocarcinoma challenge. J Urol, 1997. 158(4): pp. 1585–1588.
10.1016/S0022-5347(01)64284-8 Google Scholar
- den Brok, M.H., et al., Synergy between in situ cryoablation and TLR9 stimulation results in a highly effective in vivo dendritic cell vaccine. Cancer Res, 2006. 66(14): pp. 7285–7292.
- Riera, C.M., E.J. Brandt, and S. Shulman, Studies in cryo-immunology: IV: Antibody development in rabbits after iso-immunization followed by freezing. Immunology, 1968. 15(6): pp. 779–787.
-
Gazzaniga, S., et al., Inflammatory changes after cryosurgery-induced necrosis in human melanoma xenografted in nude mice. J Invest Dermatol, 2001. 116(5): pp. 664–671.
10.1046/j.0022-202x.2001.01313.x Google Scholar
-
Skoberne, M., A.S. Beignon, and N. Bhardwaj, Danger signals: A time and space continuum. Trends Mol Med, 2004. 10(6): pp. 251–257.
10.1016/j.molmed.2004.04.001 Google Scholar
- Peng, Y., et al., Innate and adaptive immune response to apoptotic cells. J Autoimmun, 2007. 29(4): pp. 303–309.
-
Viorritto, I.C., N.P. Nikolov, and R.M. Siegel, Autoimmunity versus tolerance: Can dying cells tip the balance? Clin Immunol, 2007. 122(2): pp. 125–134.
10.1016/j.clim.2006.07.012 Google Scholar
- Sabel, M.S., et al., Rate of freeze alters the immunologic response after cryoablation of breast cancer. Ann Surg Oncol, 2010. 17(4): pp. 1187–1193.
- Rock, K.L., et al., Natural endogenous adjuvants. Springer Semin Immunopathol, 2005. 26(3): pp. 231–246.
- Scheffer, S.R., et al., Apoptotic, but not necrotic, tumor cell vaccines induce a potent immune response in vivo. Int J Cancer, 2003. 103(2): pp. 205–211.
- Schnurr, M., et al., 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, 2002. 62(8): pp. 2347–2352.
- Benson, J.W., Regional chemotherapy and local cryotherapy for cancer. Oncology, 1972. 26(2): pp. 134–151.
- Jiang, J., et al., Tumor necrosis factor-alpha-induced accentuation in cryoinjury: Mechanisms in vitro and in vivo . Mol Cancer Ther, 2008. 7(8): pp. 2547–2555.
- Alteber, Z., et al., Cryoimmunotherapy with local co-administration of ex vivo generated dendritic cells and CpG-ODN immune adjuvant, elicits a specific antitumor immunity. Cancer Immunol Immunother, 2014. 63(4): pp. 369–380.
- den Brok, M.H., et al., Efficient loading of dendritic cells following cryo and radiofrequency ablation in combination with immune modulation induces anti-tumour immunity. Br J Cancer, 2006. 95(7): pp. 896–905.
- Waitz, R., et al., Potent induction of tumor immunity by combining tumor cryoablation with anti-CTLA-4 therapy. Cancer Res, 2012. 72(2): pp. 430–439.