Immune Effects of Cryoablation in Woodchuck Hepatocellular Carcinoma

References

• Cazzato RL, Garnon J, Ramamurthy N, et al. Percutaneous image-guided cryoablation: current applications and results in the oncologic field. Med Oncol. 2016;33:140. doi:10.1007/s12032-016-0848-3
   PubMed Web of Science ®Google Scholar
• Greten TF, Mauda-Havakuk M, Heinrich B, et al. Combined locoregional-immunotherapy for liver cancer. J Hepatol. 2019;70:999–1007. doi:10.1016/j.jhep.2019.01.027
   PubMed Web of Science ®Google Scholar
• Erinjeri JP, Fine GC, Adema GJ, et al. Immunotherapy and the interventional oncologist: challenges and opportunities-a society of interventional oncology white paper. Radiology. 2019;292:25–34. doi:10.1148/radiol.2019182326
   PubMed Web of Science ®Google Scholar
• Llovet JM, De Baere T, Kulik L, et al. Locoregional therapies in the era of molecular and immune treatments for hepatocellular carcinoma. Nat Rev Gastroenterol Hepatol. 2021;18:293–313. doi:10.1038/s41575-020-00395-0
   PubMed Web of Science ®Google Scholar
• Jansen MC, van Hillegersberg R, Schoots IG, et al. Cryoablation induces greater inflammatory and coagulative responses than radiofrequency ablation or laser induced thermotherapy in a rat liver model. Surgery. 2010;147:686–695. doi:10.1016/j.surg.2009.10.053
   PubMed Web of Science ®Google Scholar
• Chapman WC, Debelak JP, Wright Pinson C, et al. Hepatic cryoablation, but not radiofrequency ablation, results in lung inflammation. Ann Surg. 2000;231:752–761. doi:10.1097/00000658-200005000-00016
   PubMed Web of Science ®Google Scholar
• Kim GM, Won JY, Kim MD, et al. Cryoablation of hepatocellular carcinoma with high-risk for percutaneous ablation: safety and efficacy. Cardiovasc Intervent Radiol. 2016;39:1447–1454. doi:10.1007/s00270-016-1384-4
   PubMed Web of Science ®Google Scholar
• Yang WL, Addona T, Nair DG, et al. Apoptosis induced by cryo-injury in human colorectal cancer cells is associated with mitochondrial dysfunction. Int J Cancer. 2003;103:360–369. doi:10.1002/ijc.10822
   PubMed Web of Science ®Google Scholar
• Yang X, Guo Y, Guo Z, et al. Cryoablation inhibition of distant untreated tumors (abscopal effect) is immune mediated. Oncotarget. 2019;10:4180–4191. doi:10.18632/oncotarget.24105
   PubMedGoogle Scholar
• Niu L, Li J, Zeng J, et al. Comparison of percutaneous cryoablation with microwave ablation in a porcine liver model. Cryobiology. 2014;68:194–199. doi:10.1016/j.cryobiol.2014.01.005
   PubMed Web of Science ®Google Scholar
• Surtees B, Young S, Hu Y, et al. Validation of a low-cost, carbon dioxide-based cryoablation system for percutaneous tumor ablation. PLoS One. 2019;14:e0207107. doi:10.1371/journal.pone.0207107
   PubMed Web of Science ®Google Scholar
• Tennant BC, Toshkov IA, Peek SF, et al. Hepatocellular carcinoma in the woodchuck model of hepatitis B virus infection. Gastroenterology. 2004;127:S283–S93.
   PubMed Web of Science ®Google Scholar
• Roggendorf M, Kosinska AD, Liu J, Lu M. The woodchuck, a nonprimate model for immunopathogenesis and therapeutic immunomodulation in chronic hepatitis B virus infection. Cold Spring Harb Perspect Med. 2015;2015:5.
   Google Scholar
• Burke CT, Cullen JM, State A, et al. Development of an animal model for radiofrequency ablation of primary, virally induced hepatocellular carcinoma in the woodchuck. J Vasc Interv Radiol. 2011;22(1613):e1. doi:10.1016/j.jvir.2011.08.020
   Google Scholar
• Pritchard WF, Woods DL, Esparza-Trujillo JA, et al. Transarterial chemoembolization in a woodchuck model of hepatocellular carcinoma. J Vasc Interv Radiol. 2020;31:812–9.e1. doi:10.1016/j.jvir.2019.08.031
   PubMed Web of Science ®Google Scholar
• Kim AY, Yacoub JH, Field DH, et al. Suitability of the woodchuck HCC as a preclinical model for evaluation of intra-arterial therapies. Animal Model Exp Med. 2020;3:98–102. doi:10.1002/ame2.12100
   PubMedGoogle Scholar
• Wilkins LR, Stone JR, Mata J, et al. The use of the woodchuck as an animal model for evaluation of transarterial embolization. J Vasc Interv Radiol. 2017;28:1467–1471. doi:10.1016/j.jvir.2017.04.005
   PubMed Web of Science ®Google Scholar
• Mauda-Havakuk M, Mikhail AS, Starost MF, et al. Imaging, pathology, and immune correlates in the woodchuck hepatic tumor model. J Hepatocell Carcinoma. 2021;8:71–83. doi:10.2147/JHC.S287800
   PubMed Web of Science ®Google Scholar
• Esparza-Trujillo JA, Pritchard WF, Mauda-Havakuk M, et al. Imaging and pathologic evaluation of cryoablation of woodchuck (Marmota monax) hepatocellular carcinoma. Comp Med. 2023;73(2):127–133. doi:10.30802/AALAS-CM-22-000092
   PubMed Web of Science ®Google Scholar
• Mikhail AS, Mauda-Havakuk M, Partanen A, et al. Liver-specific 3D sectioning molds for correlating in vivo CT and MRI with tumor histopathology in woodchucks (Marmota monax). PLoS One. 2020;2020:15.
   Google Scholar
• Mikhail AS, Mauda-Havakuk M, Negussie AH, et al. Evaluation of immune-modulating drugs for use in drug-eluting microsphere transarterial embolization. Int J Pharm. 2022;616(121466):121466. doi:10.1016/j.ijpharm.2022.121466
   PubMedGoogle Scholar
• Roth GS, Decaens T. Liver immunotolerance and hepatocellular carcinoma: patho-physiological mechanisms and therapeutic perspectives. Eur J Cancer. 2017;87:101–112. doi:10.1016/j.ejca.2017.10.010
   PubMed Web of Science ®Google Scholar
• Ishiyama K, Ohdan H, Ohira M, et al. Difference in cytotoxicity against hepatocellular carcinoma between liver and periphery natural killer cells in humans. Hepatology. 2006;43:362–372. doi:10.1002/hep.21035
   PubMed Web of Science ®Google Scholar
• Han C, Jiang Y, Wang Z, Wang H. Natural killer cells involved in tumour immune escape of hepatocellular carcinomar. Int Immunopharmacol. 2019;73:10–16. doi:10.1016/j.intimp.2019.04.057
   PubMed Web of Science ®Google Scholar
• Waitz R, Solomon SB, Petre EN, et al. Potent induction of tumor immunity by combining tumor cryoablation with Anti-CTLA-4 Therapy. Cancer Res. 2011;72:430–439. doi:10.1158/0008-5472.CAN-11-1782
   PubMed Web of Science ®Google Scholar
• McArthur HL, Diab A, Page DB, et al. A pilot study of preoperative single-dose ipilimumab and/or cryoablation in women with early-stage breast cancer with comprehensive immune profiling. Clin Cancer Res. 2016;22:5729–5737. doi:10.1158/1078-0432.CCR-16-0190
   PubMed Web of Science ®Google Scholar
• Agdashian D, ElGindi M, Xie C, et al. The effect of anti-CTLA4 treatment on peripheral and intra-tumoral T cells in patients with hepatocellular carcinoma. Cancer Immunol Immunother. 2019;68:599–608. doi:10.1007/s00262-019-02299-8
   PubMed Web of Science ®Google Scholar
• Yakkala C, Chiang CL, Kandalaft L, et al. Cryoablation and Immunotherapy: an enthralling synergy to confront the tumors. Front Immunol. 2019;10:2283. doi:10.3389/fimmu.2019.02283
   PubMed Web of Science ®Google Scholar
• Redondo P, Del Olmo J, Lopez-Diaz de Cerio A, et al. Imiquimod enhances the systemic immunity attained by local cryosurgery destruction of melanoma lesions. J Invest Dermatol. 2007;127:1673–1680. doi:10.1038/sj.jid.5700777
   PubMed Web of Science ®Google Scholar
• Ahmed M, Kumar G, Moussa M, et al. Hepatic radiofrequency ablation-induced stimulation of distant tumor growth is suppressed by c-met inhibition. Radiology. 2016;279:103–117. doi:10.1148/radiol.2015150080
   PubMed Web of Science ®Google Scholar
• Ahmed M, Kumar G, Gourevitch S, et al. Radiofrequency ablation (RFA)-induced systemic tumor growth can be reduced by suppression of resultant heat shock proteins. Int J Hyperthermia. 2018;34:934–942. doi:10.1080/02656736.2018.1462535
   PubMed Web of Science ®Google Scholar
• Tanis E, Nordlinger B, Mauer M, et al. Local recurrence rates after radiofrequency ablation or resection of colorectal liver metastases. Analysis of the European organisation for research and treatment of cancer #40004 and #40983. Eur J Cancer. 2014;50:912–919. doi:10.1016/j.ejca.2013.12.008
   PubMed Web of Science ®Google Scholar
• Shi L, Wang J, Ding N, et al. Inflammation induced by incomplete radiofrequency ablation accelerates tumor progression and hinders PD-1 immunotherapy. Nat Commun. 2019;10:5421. doi:10.1038/s41467-019-13204-3
   PubMed Web of Science ®Google Scholar
• Wing MG, Rogers K, Jacob G, Rees RC. Characterisation of suppressor cells generated following cryosurgery of an HSV-2-induced fibrosarcoma. Cancer Immunol Immunother. 1988;26:169–175. doi:10.1007/BF00205611
   PubMed Web of Science ®Google Scholar
• Helmberger T. The evolution of interventional oncology in the 21st century. Br J Radiol. 2020;93:20200112. doi:10.1259/bjr.20200112
   PubMed Web of Science ®Google Scholar
• Shao Q, O’Flanagan S, Lam T, et al. Engineering T cell response to cancer antigens by choice of focal therapeutic conditions. Int J Hyperthermia. 2019;36:130–138. doi:10.1080/02656736.2018.1539253
   PubMed Web of Science ®Google Scholar
• Hou J, Zhang H, Sun B, Karin M. The immunobiology of hepatocellular carcinoma in humans and mice: basic concepts and therapeutic implications. J Hepatol. 2020;72:167–182. doi:10.1016/j.jhep.2019.08.014
   PubMed Web of Science ®Google Scholar
• Lawal G, Xiao Y, Rahnemai-Azar AA, et al. The immunology of hepatocellular carcinoma. Vaccines. 2021;9:1184. doi:10.3390/vaccines9101184
   Web of Science ®Google Scholar
• Gamrekelashvili J, Kruger C, von Wasielewski R, et al. Necrotic tumor cell death in vivo impairs tumor-specific immune responses. J Immunol. 2007;178:1573–1580. doi:10.4049/jimmunol.178.3.1573
   PubMed Web of Science ®Google Scholar
• Janke LJ, Ward JM, Vogel P. Classification, scoring, and quantification of cell death in tissue sections. Vet Pathol. 2019;56:33–38. doi:10.1177/0300985818800026
   PubMed Web of Science ®Google Scholar