Incomplete thermal ablation of tumors promotes increased tumorigenesis

References

• Solbiati L, Ahmed M, Cova L, et al. Small liver colorectal metastases treated with percutaneous radiofrequency ablation: local response rate and long-term survival with up to 10-year follow-up. Radiology. 2012;265:958–968.
   PubMed Web of Science ®Google Scholar
• Meloni MF, Andreano A, Laeseke PF, et al. Breast cancer liver metastases: US-guided percutaneous radiofrequency ablation-intermediate and long-term survival rates . Radiology. 2009;253:861–869.
   PubMed Web of Science ®Google Scholar
• EASL-EORTC. EASL-EORTC clinical practice guidelines: management of hepatocellular carcinoma. J Hepatol. 2012;56:908–943.
   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.
   PubMed Web of Science ®Google Scholar
• Rozenblum N, Zeira E, Scaiewicz V, et al. Oncogenesis: an "off-target" effect of radiofrequency ablation. Radiology. 2015;276:426–432.
   PubMed Web of Science ®Google Scholar
• Thompson SM, Jondal DE, Butters KA, et al. Heat stress and thermal ablation induce local expression of nerve growth factor inducible (VGF) in hepatocytes and hepatocellular carcinoma: pre-clinical and clinical studies. Gene Expr. 2018;19:37–47.
   PubMedGoogle Scholar
• Nijkamp MW, Borren A, Govaert KM, et al. Radiofrequency ablation of colorectal liver metastases induces an inflammatory response in distant hepatic metastases but not in local accelerated outgrowth. J Surg Oncol. 2010;101:551–556.
   PubMed Web of Science ®Google Scholar
• Nijkamp MW, van der Bilt JD, de Bruijn MT, et al. Accelerated perinecrotic outgrowth of colorectal liver metastases following radiofrequency ablation is a hypoxia-driven phenomenon. Ann Surg. 2009;249:814–823.
   PubMed Web of Science ®Google Scholar
• Erinjeri JP, Thomas CT, Samoilia A, et al. Image-guided thermal ablation of tumors increases the plasma level of interleukin-6 and interleukin-10. J Vasc Interv Radiol. 2013;24:1105–1112.
   PubMed Web of Science ®Google Scholar
• Hinz S, Tepel J, Roder C, et al. Profile of serum factors and disseminated tumor cells before and after radiofrequency ablation compared to resection of colorectal liver metastases – a pilot study. Anticancer Res. 2015;35:2961–2967.
   PubMed Web of Science ®Google Scholar
• Ahmed M, Kumar G, Navarro G, et al. Systemic siRNA nanoparticle-based drugs combined with radiofrequency ablation for cancer therapy. Plos One. 2015;10:e0128910.
   PubMed Web of Science ®Google Scholar
• Rozenblum N, Zeira E, Bulvik B, et al. Radiofrequency ablation: inflammatory changes in the periablative zone can induce global organ effects, including liver regeneration. Radiology. 2015;276:416–425.
   PubMed Web of Science ®Google Scholar
• Yang W, Ahmed M, Tasawwar B, et al. Combination radiofrequency (RF) ablation and IV liposomal heat shock protein suppression: reduced tumor growth and increased animal endpoint survival in a small animal tumor model. J Control Release. 2012;160:239–244.
   PubMed Web of Science ®Google Scholar
• Ahmed M, Monsky WE, Girnun G, et al. Radiofrequency thermal ablation sharply increases intratumoral liposomal doxorubicin accumulation and tumor coagulation. Cancer Res. 2003;63:6327–6333.
   PubMed Web of Science ®Google Scholar
• Monsky WL, Kruskal JB, Lukyanov AN, et al. Radio-frequency ablation increases intratumoral liposomal doxorubicin accumulation in a rat breast tumor model. Radiology. 2002;224:823–829.
   PubMed Web of Science ®Google Scholar
• Solazzo SA, Ahmed M, Schor-Bardach R, et al. Liposomal doxorubicin increases radiofrequency ablation-induced tumor destruction by increasing cellular oxidative and nitrative stress and accelerating apoptotic pathways. Radiology. 2010;255:62–74.
   PubMed Web of Science ®Google Scholar
• Abarbanell AM, Wang Y, Herrmann JL, et al. Toll-like receptor 2 mediates mesenchymal stem cell-associated myocardial recovery and VEGF production following acute ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol. 2010;298:H1529–H1536.
   PubMed Web of Science ®Google Scholar
• Sotirchos VS, Petrovic LM, Gonen M, et al. Colorectal cancer liver metastases: biopsy of the ablation zone and margins can be used to predict oncologic outcome. Radiology. 2016;280:949–959.
   PubMed Web of Science ®Google Scholar
• Snoeren N, Huiskens J, Rijken AM, et al. Viable tumor tissue adherent to needle applicators after local ablation: a risk factor for local tumor progression. Ann Surg Oncol. 2011;18:3702–3710.
   PubMed Web of Science ®Google Scholar
• Ang CS, Sun MY, Huitzil-Melendez DF, et al. c-MET and HGF mRNA expression in hepatocellular carcinoma: correlation with clinicopathological features and survival. Anticancer Res. 2013;33:3241–3245.
   PubMed Web of Science ®Google Scholar
• Dankbar B, Padro T, Leo R, et al. Vascular endothelial growth factor and interleukin-6 in paracrine tumor-stromal cell interactions in multiple myeloma. Blood. 2000;95:2630–2636.
   PubMed Web of Science ®Google Scholar
• Gherardi E, Birchmeier W, Birchmeier C, et al. Targeting MET in cancer: rationale and progress. Nat Rev Cancer. 2012;12:89–103.
   PubMed Web of Science ®Google Scholar
• Goyal L, Muzumdar MD, Zhu AX. Targeting the HGF/c-MET pathway in hepatocellular carcinoma. Clin Cancer Res. 2013;19:2310–2318.
   PubMed Web of Science ®Google Scholar
• Middleton K, Jones J, Lwin Z, et al. Interleukin-6: an angiogenic target in solid tumours. Crit Rev Oncol Hematol. 2014;89:129–139.
   PubMed Web of Science ®Google Scholar
• Mittal K, Ebos J, Rini B. Angiogenesis and the tumor microenvironment: vascular endothelial growth factor and beyond. Semin Oncol. 2014;41:235–251.
   PubMed Web of Science ®Google Scholar
• Sun R, Jaruga B, Kulkarni S, et al. IL-6 modulates hepatocyte proliferation via induction of HGF/p21cip1: regulation by SOCS3. Biochem Biophys Res Commun. 2005;338:1943–1949.
   PubMed Web of Science ®Google Scholar
• Thompson SM, Callstrom MR, Jondal DE, et al. Heat stress-induced PI3K/mTORC2-dependent AKT signaling is a central mediator of hepatocellular carcinoma survival to thermal ablation induced heat stress. PLoS One. 2016;11:e0162634.
   PubMed Web of Science ®Google Scholar
• Yang W, Ahmed M, Tasawwar B, et al. Radiofrequency ablation combined with liposomal quercetin to increase tumour destruction by modulation of heat shock protein production in a small animal model. Int J Hyperthermia. 2011;27:527–538.
   PubMed Web of Science ®Google Scholar
• Shady W, Petre EN, Vakiani E, et al. Kras mutation is a marker of worse oncologic outcomes after percutaneous radiofrequency ablation of colorectal liver metastases. Oncotarget. 2017;8:66117–66127.
   PubMedGoogle Scholar
• Bruenn K, Beyer L, Haimerl M, et al. Comparison of computed tomography (CT) and contrast-enhanced ultrasound (CEUS) for the quantitative evaluation of an ablation defect following radiofrequency ablation of malignant liver lesions. Clin Hemorheol Microcirc. 2017;67:445–451.
   PubMed Web of Science ®Google Scholar
• Bulvik BE, Rozenblum N, Gourevich S, et al. Irreversible electroporation versus radiofrequency ablation: a comparison of local and systemic effects in a small-animal model. Radiology. 2016;280:413–424.
   PubMed Web of Science ®Google Scholar
• Velez E, Goldberg SN, Kumar G, et al. Hepatic thermal ablation: effect of device and heating parameters on local tissue reactions and distant tumor growth. Radiology. 2016;281:782–792.
   PubMed Web of Science ®Google Scholar