Thermal ablation of pancreatic cancer: A systematic literature review of clinical practice and pre-clinical studies

Abstract Purpose: Pancreatic cancer is a challenging malignancy with low treatment option and poor life expectancy. Thermal ablation techniques were proposed as alternative treatment options, especially in advanced stages and for unfit-for-surgery patients. This systematic review describes the thermal ablative techniques -i.e., Laser (LA), Radiofrequency (RFA), Microwave (MWA) Ablation, High-Intensity Focused Ultrasound (HIFU) and cryoablation- available for pancreatic cancer treatment. Additionally, an analysis of the efficacy, complication rate and overall survival for each technique is conducted. Material and methods: This review collects the ex vivo, preclinical and clinical studies presenting the use of thermal techniques in the pancreatic cancer treatment, searched up to March 2018 in PubMed and Medline. Abstracts, letters-to-the-editor, expert opinions, reviews and non-English language manuscripts were excluded. Results: Sixty-five papers were included. For the ex vivo and preclinical studies, there are: 12 records for LA, 8 for RFA, 0 for MWA, 6 for HIFU, 1 for cryoablation and 3 for hybrid techniques. For clinical studies, 1 paper for LA, 14 for RFA, 1 for MWA, 17 for HIFU, 1 for cryoablation and 1 for hybrid techniques. Conclusions: Important technological advances are presented in ex vivo and preclinical studies, as the real-time thermometry, nanotechnology and hybrid techniques to enhance the thermal outcome. Conversely, a lack of standardization in the clinical employment of the procedures emerged, leading to contrasting results on the safety and feasibility of some analyzed techniques. Uniform conclusions on the safety and feasibility of these techniques for pancreatic cancer will require further structured investigation.

[1]  J. Knox,et al.  Locally advanced pancreatic cancer: An emerging entity. , 2017, Current problems in cancer.

[2]  David Goldstein,et al.  Effect of Chemoradiotherapy vs Chemotherapy on Survival in Patients With Locally Advanced Pancreatic Cancer Controlled After 4 Months of Gemcitabine With or Without Erlotinib: The LAP07 Randomized Clinical Trial. , 2016, JAMA.

[3]  Sergio Silvestri,et al.  US-guided application of Nd:YAG laser in porcine pancreatic tissue: an ex vivo study and numerical simulation. , 2013, Gastrointestinal endoscopy.

[4]  L. Schwartz,et al.  New response evaluation criteria in solid tumours: revised RECIST guideline (version 1.1). , 2009, European journal of cancer.

[5]  Jin Hee Jang,et al.  High-intensity focused ultrasound ablation in hepatic and pancreatic cancer: complications , 2011, Abdominal Imaging.

[6]  C. Doglioni,et al.  US-guided application of a new hybrid probe in human pancreatic adenocarcinoma: an ex vivo study. , 2010, Gastrointestinal endoscopy.

[7]  R. van Hillegersberg,et al.  Radiofrequency ablation of the pancreas: two-week follow-up in a porcine model. , 2014, European journal of surgical oncology : the journal of the European Society of Surgical Oncology and the British Association of Surgical Oncology.

[8]  J. Lovelock,et al.  The haemolysis of human red blood-cells by freezing and thawing. , 1953, Biochimica et biophysica acta.

[9]  B. Hooper Optical-thermal response of laser-irradiated tissue , 1996 .

[10]  A. Biankin,et al.  Chemotherapy and radiotherapy for advanced pancreatic cancer. , 2018, The Cochrane database of systematic reviews.

[11]  P. Hadjicostas,et al.  Radiofrequency ablation in pancreatic cancer. , 2006, HPB : the official journal of the International Hepato Pancreato Biliary Association.

[12]  V. Cicinnati,et al.  Endoscopic ultrasound guided radiofrequency ablation, for pancreatic cystic neoplasms and neuroendocrine tumors. , 2015, World journal of gastrointestinal surgery.

[13]  J. Erinjeri,et al.  Cryoablation: mechanism of action and devices. , 2010, Journal of vascular and interventional radiology : JVIR.

[14]  F. X. Roux,et al.  Interstitial laser thermotherapy in neurosurgery: A review , 2005, Acta Neurochirurgica.

[15]  Yan Liu,et al.  High-intensity focused ultrasound treatment for patients with unresectable pancreatic cancer. , 2012, Hepatobiliary & pancreatic diseases international : HBPD INT.

[16]  C. Bassi,et al.  Percutaneous Radiofrequency Ablation of Unresectable Locally Advanced Pancreatic Cancer: Preliminary Results , 2017, Technology in cancer research & treatment.

[17]  W. Ma,et al.  Contemporary Management of Localized Resectable Pancreatic Cancer , 2018, Cancers.

[18]  J. Vidal-Jové,et al.  Ultrasound Guided High Intensity Focused Ultrasound for malignant tumors: The Spanish experience of survival advantage in stage III and IV pancreatic cancer. , 2015, Ultrasonics sonochemistry.

[19]  Wayne Kreider,et al.  Passive cavitation detection during pulsed HIFU exposures of ex vivo tissues and in vivo mouse pancreatic tumors. , 2014, Ultrasound in medicine & biology.

[20]  Jae Young Lee,et al.  Dynamic contrast–enhanced ultrasonographic (DCE-US) assessment of the early response after combined gemcitabine and HIFU with low-power treatment for the mouse xenograft model of human pancreatic cancer , 2014, European Radiology.

[21]  S. Yoon,et al.  Long-Term Outcome of High-Intensity Focused Ultrasound in Advanced Pancreatic Cancer , 2011, Pancreas.

[22]  Robert Carlisle,et al.  Ultrasound-enhanced drug delivery for cancer , 2012, Expert opinion on drug delivery.

[23]  F. Lee,et al.  Radiofrequency versus microwave ablation in a hepatic porcine model. , 2005, Radiology.

[24]  Eun Sun Lee,et al.  Pulsed high-intensity focused ultrasound enhances apoptosis of pancreatic cancer xenograft with gemcitabine. , 2013, Ultrasound in medicine & biology.

[25]  Rafael Duran,et al.  Efficacy of microwave ablation versus radiofrequency ablation for the treatment of hepatocellular carcinoma in patients with chronic liver disease: a randomised controlled phase 2 trial. , 2018, The lancet. Gastroenterology & hepatology.

[26]  A. Siriwardena,et al.  Development and Validation of an Experimental Model for the Assessment of Radiofrequency Ablation of Pancreatic Parenchyma , 2005, Pancreas.

[27]  G. Gazelle,et al.  EUS-guided radiofrequency ablation in the pancreas: results in a porcine model. , 1999, Gastrointestinal endoscopy.

[28]  Sergio Silvestri,et al.  Feasibility of EUS-guided Nd:YAG laser ablation of unresectable pancreatic adenocarcinoma. , 2018, Gastrointestinal endoscopy.

[29]  C. Strassburg,et al.  High-intensity focused ultrasound (HIFU) for pancreatic carcinoma: evaluation of feasibility, reduction of tumour volume and pain intensity , 2016, European Radiology.

[30]  E. Berjano,et al.  Radiofrequency Pancreatic Ablation and Section of the Main Pancreatic Duct Does Not Lead to Necrotizing Pancreatitis , 2014 .

[31]  Sergio Silvestri,et al.  Laser Interstitial Thermotherapy for pancreatic tumor ablation: Theoretical model and experimental validation , 2011, 2011 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[32]  N. Yamanaka,et al.  Optimal combination of radiofrequency ablation with chemoradiotherapy for locally advanced pancreatic cancer. , 2012, World journal of clinical oncology.

[33]  Sergio Silvestri,et al.  EUS-guided Nd:YAG laser ablation of normal pancreatic tissue: a pilot study in a pig model. , 2010, Gastrointestinal endoscopy.

[34]  Carlo Fugazzola,et al.  Microwave ablation of pancreatic head cancer: safety and efficacy. , 2013, Journal of Vascular and Interventional Radiology.

[35]  E. Schena,et al.  Laser Ablation for Cancer: Past, Present and Future , 2017, Journal of functional biomaterials.

[36]  Wen Chen,et al.  High-intensity focused ultrasound treatment of late-stage pancreatic body carcinoma: optimal tumor depth for safe ablation. , 2014, Ultrasound in medicine & biology.

[37]  Ke-cheng Xu,et al.  Advances in cryoablation for pancreatic cancer. , 2016, World journal of gastroenterology.

[38]  Wen-Zhi Chen,et al.  Feasibility of US-guided high-intensity focused ultrasound treatment in patients with advanced pancreatic cancer: initial experience. , 2005, Radiology.

[39]  Hui Zhu,et al.  High-intensity focused ultrasound (HIFU): effective and safe therapy for hepatocellular carcinoma adjacent to major hepatic veins , 2009, European Radiology.

[40]  D. Dupuy,et al.  Thermal ablation of tumours: biological mechanisms and advances in therapy , 2014, Nature Reviews Cancer.

[41]  F. Itokawa,et al.  The current potential of high-intensity focused ultrasound for pancreatic carcinoma , 2011, Journal of hepato-biliary-pancreatic sciences.

[42]  N N Korpan Cryosurgery: Ultrastructural Changes in Pancreas Tissue after Low Temperature Exposure , 2007, Technology in cancer research & treatment.

[43]  Ashleyj . Welch,et al.  Optical-Thermal Response of Laser-Irradiated Tissue , 1995 .

[44]  Ciprian Lucan,et al.  Selective ex-vivo photothermal ablation of human pancreatic cancer with albumin functionalized multiwalled carbon nanotubes , 2011, International journal of nanomedicine.

[45]  F. Starr,et al.  Preclinical in vivo evaluation of an extracorporeal HIFU device for ablation of pancreatic tumors. , 2009, Ultrasound in medicine & biology.

[46]  Lihua He,et al.  Combination Treatment With Comprehensive Cryoablation and Immunotherapy in Metastatic Pancreatic Cancer , 2013, Pancreas.

[47]  S. Nahum Goldberg,et al.  Radiofrequency tumor ablation: principles and techniques , 2001 .

[48]  E Schena,et al.  Magnetic resonance-based thermometry during laser ablation on ex-vivo swine pancreas and liver. , 2015, Medical engineering & physics.

[49]  Sergio Silvestri,et al.  Theoretical assessment of principal factors influencing laser interstitial thermotherapy outcomes on pancreas , 2012, 2012 Annual International Conference of the IEEE Engineering in Medicine and Biology Society.

[50]  C. Catalano,et al.  Nonoperative Ablation of Pancreatic Neoplasms. , 2018, The Surgical clinics of North America.

[51]  R. Stafford,et al.  Nanoshell-mediated near-infrared thermal therapy of tumors under magnetic resonance guidance , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[52]  Emiliano Schena,et al.  Assessment of temperature measurement error and its correction during Nd:YAG laser ablation in porcine pancreas , 2014, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[53]  Kun Wang,et al.  Safety Evaluation of High-Intensity Focused Ultrasound in Patients with Pancreatic Cancer , 2013, Oncology Research and Treatment.

[54]  C. Bassi,et al.  Percutaneous ablation of pancreatic cancer , 2016, World journal of gastroenterology.

[55]  Sergio Silvestri,et al.  Theoretical Analysis and Experimental Evaluation of Laser-Induced Interstitial Thermotherapy in Ex Vivo Porcine Pancreas , 2012, IEEE Transactions on Biomedical Engineering.

[56]  Teodora Mocan,et al.  Photothermal Treatment of Human Pancreatic Cancer Using PEGylated Multi-Walled Carbon Nanotubes Induces Apoptosis by Triggering Mitochondrial Membrane Depolarization Mechanism , 2014, Journal of Cancer.

[57]  C. Moskaluk,et al.  Endoscopic Ultrasound-Guided Radiofrequency Ablation (EUS-RFA) of the Pancreas in a Porcine Model , 2012, Gastroenterology research and practice.

[58]  C. Doglioni,et al.  Endoscopic ultrasound-guided application of a new hybrid cryotherm probe in porcine pancreas: a preliminary study , 2008, Endoscopy.

[59]  J. Marescaux,et al.  Thermal Treatments of Tumors , 2018 .

[60]  K. T. Moesta,et al.  Histopathological Correlation to MRI Findings During and After Laser-Induced Thermotherapy in a Pig Pancreas Model , 2001, Investigative radiology.

[61]  Pierre Michel,et al.  FOLFIRINOX versus gemcitabine for metastatic pancreatic cancer. , 2011, The New England journal of medicine.

[62]  Kemal Tuncali,et al.  Percutaneous cryoablation techniques and clinical applications. , 2010, Diagnostic and interventional radiology.

[63]  C. Bassi,et al.  Variation of tumoral marker after radiofrequency ablation of pancreatic adenocarcinoma. , 2016, Journal of gastrointestinal oncology.

[64]  N. Michalopoulos,et al.  Radiofrequency ablation combined with palliative surgery may prolong survival of patients with advanced cancer of the pancreas , 2006, Langenbeck's Archives of Surgery.

[65]  A. Facciorusso,et al.  Microwave ablation versus radiofrequency ablation for the treatment of hepatocellular carcinoma: A systematic review and meta-analysis , 2016, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[66]  Umberto Veronesi,et al.  High-intensity focused ultrasound ablation: effective and safe therapy for solid tumors in difficult locations. , 2010, AJR. American journal of roentgenology.

[67]  E. Touboul,et al.  Impact of chemoradiotherapy after disease control with chemotherapy in locally advanced pancreatic adenocarcinoma in GERCOR phase II and III studies. , 2007, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[68]  R. van Hillegersberg,et al.  Radiofrequency ablation for unresectable locally advanced pancreatic cancer: a systematic review. , 2014, HPB : the official journal of the International Hepato Pancreato Biliary Association.

[69]  R. Barr,et al.  Contrast-Enhanced Ultrasound-Guided Radiofrequency Ablation of Renal Tumors , 2018, Journal of kidney cancer and VHL.

[70]  Thomas Schmitz-Rode,et al.  Multi-slice computed tomography: A tool for non-invasive temperature measurement? , 2010, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[71]  Lianyu Chen,et al.  Analgesic effect of high intensity focused ultrasound therapy for unresectable pancreatic cancer , 2011, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[72]  John G. Webster,et al.  A floating sleeve antenna yields localized hepatic microwave ablation , 2006, IEEE Transactions on Biomedical Engineering.

[73]  J. Herman,et al.  Stereotactic Radiotherapy and Particle Therapy for Pancreatic Cancer , 2018, Cancers.

[74]  F V Gleeson,et al.  The safety and feasibility of extracorporeal high-intensity focused ultrasound (HIFU) for the treatment of liver and kidney tumours in a Western population , 2005, British Journal of Cancer.

[75]  Douglas B. Evans,et al.  Induction chemotherapy selects patients with locally advanced, unresectable pancreatic cancer for optimal benefit from consolidative chemoradiation therapy , 2007, Cancer.

[76]  Jeffrey E. Lee,et al.  Borderline Resectable Pancreatic Cancer: Definitions, Management, and Role of Preoperative Therapy , 2006, Annals of Surgical Oncology.

[77]  S. Curley,et al.  Tumor Selective Hyperthermia Induced by Short-Wave Capacitively-Coupled RF Electric-Fields , 2013, PloS one.

[78]  Emiliano Schena,et al.  Gold nanorod-mediated near-infrared laser ablation: in vivo experiments on mice and theoretical analysis at different settings , 2017, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[79]  Y. Zou,et al.  Intraoperative radiofrequency ablation combined with 125 iodine seed implantation for unresectable pancreatic cancer. , 2010, World journal of gastroenterology.

[80]  D. Ryan,et al.  Adjuvant therapy for pancreatic cancer , 2008, Cancer.

[81]  A. Vercelli,et al.  Radiofrequency Ablation of Pancreatic Neuroendocrine Tumors: A Pilot Study of Feasibility, Efficacy, and Safety , 2014, Pancreas.

[82]  Glenn P. Goodrich,et al.  Initial Evaluation of the Safety of Nanoshell-Directed Photothermal Therapy in the Treatment of Prostate Disease , 2016, International journal of toxicology.

[83]  A. Villers,et al.  Target ablation--image-guided therapy in prostate cancer. , 2014, Urologic oncology.

[84]  N. Yamanaka,et al.  Effectiveness of impedance monitoring during radiofrequency ablation for predicting popping. , 2012, World journal of gastroenterology.

[85]  M. Anzidei,et al.  Magnetic Resonance-Guided Focused Ultrasound Ablation in Abdominal Moving Organs: A Feasibility Study in Selected Cases of Pancreatic and Liver Cancer , 2014, CardioVascular and Interventional Radiology.

[86]  E. Petre,et al.  Thermal Ablation in the Management of Colorectal Cancer Patients with Oligometastatic Liver Disease , 2017, Visceral Medicine.

[87]  F. Orsi,et al.  High-intensity focused ultrasound (HIFU) in patients with solid malignancies: evaluation of feasibility, local tumour response and clinical results , 2011, La radiologia medica.

[88]  D. Haemmerich,et al.  Review of temperature dependence of thermal properties, dielectric properties, and perfusion of biological tissues at hyperthermic and ablation temperatures. , 2014, Critical reviews in biomedical engineering.

[89]  D. Dimitroulopoulos,et al.  Gemcitabine as palliative treatment in patients with unresectable pancreatic cancer previously treated with placement of a covered metal stent. A randomized controlled trial. , 2008, Journal of B.U.ON. : official journal of the Balkan Union of Oncology.

[90]  A. Biankin,et al.  Targeted therapies in the management of locally advanced and metastatic pancreatic cancer: a systematic review , 2018, Oncotarget.

[91]  E Schena,et al.  Experimental assessment of CT-based thermometry during laser ablation of porcine pancreas , 2013, Physics in medicine and biology.

[92]  N. Reddy,et al.  Initial experience of EUS-guided radiofrequency ablation of unresectable pancreatic cancer. , 2015, Gastrointestinal endoscopy.

[93]  S. Varshney,et al.  Radiofrequency ablation of unresectable pancreatic carcinoma: feasibility, efficacy and safety. , 2006, JOP : Journal of the pancreas.

[94]  H. Schild,et al.  Clinical Use of High-Intensity Focused Ultrasound (HIFU) for Tumor and Pain Reduction in Advanced Pancreatic Cancer , 2016, Fortschritte auf dem Gebiet der Röntgenstrahlen und der bildgebenden Verfahren.

[95]  S. Pereira,et al.  Successful management of a sporadic pancreatic insulinoma by endoscopic ultrasound-guided radiofrequency ablation , 2016, Endoscopy.

[96]  M. Reni,et al.  Feasibility and safety of EUS-guided cryothermal ablation in patients with locally advanced pancreatic cancer. , 2012, Gastrointestinal endoscopy.

[97]  U. G. Dailey Cancer,Facts and Figures about. , 2022, Journal of the National Medical Association.

[98]  Yu-jiang Li,et al.  The combination therapy of high-intensity focused ultrasound with radiotherapy in locally advanced pancreatic carcinoma , 2016, World Journal of Surgical Oncology.

[99]  Tibor Schuster,et al.  Preoperative/Neoadjuvant Therapy in Pancreatic Cancer: A Systematic Review and Meta-analysis of Response and Resection Percentages , 2010, PLoS medicine.

[100]  Philippe L Pereira,et al.  Radiofrequency ablation: in vivo comparison of four commercially available devices in pig livers. , 2004, Radiology.

[101]  Yang Guo,et al.  Photothermal ablation of pancreatic cancer cells with hybrid iron-oxide core gold-shell nanoparticles , 2013, International journal of nanomedicine.

[102]  Osama Al-Bataineh,et al.  Clinical and future applications of high intensity focused ultrasound in cancer. , 2012, Cancer treatment reviews.

[103]  Sebastien Crouzet,et al.  High intensity focused ultrasound (HIFU) for prostate cancer: Current clinical status, outcomes and future perspectives , 2010, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[104]  Lin Jia,et al.  Experimental ablation of the pancreas with high intensity focused ultrasound (HIFU) in a porcine model , 2010, International journal of medical sciences.

[105]  Tong Li,et al.  Endoscopic high-intensity focused US: technical aspects and studies in an in vivo porcine model (with video). , 2015, Gastrointestinal endoscopy.

[106]  Ho Kim,et al.  EUS-guided radiofrequency ablation of the porcine pancreas. , 2011, Gastrointestinal endoscopy.

[107]  S. Lakhtakia,et al.  EUS-guided radiofrequency ablation for management of pancreatic insulinoma by using a novel needle electrode (with videos). , 2016, Gastrointestinal endoscopy.

[108]  Jae Young Lee,et al.  Concurrent Chemotherapy and Pulsed High-Intensity Focused Ultrasound Therapy for the Treatment of Unresectable Pancreatic Cancer: Initial Experiences , 2011, Korean journal of radiology.

[109]  G. Dodd,et al.  Effect of variation of portal venous blood flow on radiofrequency and microwave ablations in a blood-perfused bovine liver model. , 2013, Radiology.

[110]  J. Hwang,et al.  HIFU for Palliative Treatment of Pancreatic Cancer. , 2011, Advances in experimental medicine and biology.

[111]  Guowang Yang,et al.  Concurrent gemcitabine and high-intensity focused ultrasound therapy in patients with locally advanced pancreatic cancer , 2010, Anti-cancer drugs.

[112]  A. Siriwardena,et al.  Radiofrequency ablation of the pancreas. I: Definition of optimal thermal kinetic parameters and the effect of simulated portal venous circulation in an ex-vivo porcine model. , 2005, JOP : Journal of the pancreas.

[113]  Emiliano Schena,et al.  Endoscopic ultrasound-guided Nd:YAG laser ablation of recurrent pancreatic neuroendocrine tumor: a promising revolution? , 2014, Endoscopy.

[114]  N. Habib,et al.  Analysis of Endoscopic Radiofrequency Ablation of Biliary Malignant Strictures in Pancreatic Cancer Suggests Potential Survival Benefit , 2015, Digestive Diseases and Sciences.

[115]  Matthew S. Adams,et al.  Endoluminal ultrasound applicators for MR-guided thermal ablation of pancreatic tumors: Preliminary design and evaluation in a porcine pancreas model. , 2016, Medical physics.

[116]  Guojing Wang,et al.  Preoperative ultrasound ablation for borderline resectable pancreatic cancer: A report of 30 cases. , 2015, Ultrasonics sonochemistry.

[117]  Hui Zhu,et al.  High intensity focused ultrasound (HIFU) therapy for local treatment of hepatocellular carcinoma: role of partial rib resection. , 2009, European journal of radiology.

[118]  C. Bassi,et al.  Triple approach strategy for patients with locally advanced pancreatic carcinoma. , 2013, HPB.