Equivalence of cell survival data for radiation dose and thermal dose in ablative treatments: analysis applied to essential tremor thalamotomy by focused ultrasound and gamma knife

Abstract Thermal dose and absorbed radiation dose have historically been difficult to compare because different biological mechanisms are at work. Thermal dose denatures proteins and the radiation dose causes DNA damage in order to achieve ablation. The purpose of this paper is to use the proportion of cell survival as a potential common unit by which to measure the biological effect of each procedure. Survival curves for both thermal and radiation doses have been extracted from previously published data for three different cell types. Fits of these curves were used to convert both thermal and radiation dose into the same quantified biological effect: fraction of surviving cells. They have also been used to generate and compare survival profiles from the only indication for which clinical data are available for both focused ultrasound (FUS) thermal ablation and radiation ablation: essential tremor thalamotomy. All cell types could be fitted with coefficients of determination greater than 0.992. As an illustration, survival profiles of clinical thalamotomies performed by radiosurgery and FUS are plotted on a same graph for the same metric: fraction of surviving cells. FUS and Gamma Knife have the potential to be used in combination to deliver a more effective treatment (for example, FUS may be used to debulk the main tumour mass, and radiation to treat the surrounding tumour bed). In this case, a model which compares thermal and radiation treatments is valuable in order to adjust the dose between the two.

[1]  G. Barnett,et al.  Stereotactic laser ablation as treatment for brain metastases that recur after stereotactic radiosurgery: a multiinstitutional experience. , 2016, Neurosurgical focus.

[2]  Charles B Simone,et al.  Therapeutic hyperthermia: The old, the new, and the upcoming. , 2016, Critical reviews in oncology/hematology.

[3]  J. Antolak The Physics of Radiation Therapy , 2015 .

[4]  I. Rivens,et al.  A study of thermal dose-induced autophagy, apoptosis and necroptosis in colon cancer cells , 2015, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[5]  D. Pavord,et al.  Practical Radiation Oncology Physics : A Companion to Gunderson and Tepper's Clinical Radiation Oncology , 2015 .

[6]  G. V. van Rhoon,et al.  Development of a novel method to enhance the therapeutic effect on tumours by simultaneous action of radiation and heating , 2015, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[7]  Joo Ha Hwang,et al.  Emerging HIFU applications in cancer therapy , 2015, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[8]  M. Story,et al.  An Experimental Model-Based Exploration of Cytokines in Ablative Radiation-Induced Lung Injury In Vivo and In Vitro , 2015, Lung.

[9]  E. Ebbini,et al.  Ultrasound-guided therapeutic focused ultrasound: Current status and future directions , 2015, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[10]  John M Gorman,et al.  Rationalization of thermal injury quantification methods: application to skin burns. , 2014, Burns : journal of the International Society for Burn Injuries.

[11]  J. Sonke,et al.  Alpha/beta ratio for normal lung tissue as estimated from lung cancer patients treated with stereotactic body and conventionally fractionated radiation therapy. , 2014, International journal of radiation oncology, biology, physics.

[12]  F. Jolesz,et al.  Nonthermal ablation with microbubble-enhanced focused ultrasound close to the optic tract without affecting nerve function. , 2013, Journal of neurosurgery.

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

[14]  Max Wintermark,et al.  A pilot study of focused ultrasound thalamotomy for essential tremor. , 2013, The New England journal of medicine.

[15]  Jean-François Aubry,et al.  Image-guided focused ultrasound: state of the technology and the challenges that lie ahead , 2013 .

[16]  John A. Pearce,et al.  Comparative analysis of mathematical models of cell death and thermal damage processes , 2013, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[17]  K. Camphausen,et al.  Preclinical models in radiation oncology , 2012, Radiation Oncology.

[18]  M. Weinmann,et al.  Pathological complete response and sphincter-sparing surgery after neoadjuvant radiochemotherapy with regional hyperthermia for locally advanced rectal cancer compared with radiochemotherapy alone , 2012, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[19]  D. Dupuy,et al.  Microwave ablation for lung cancer. , 2012, Medicine and health, Rhode Island.

[20]  M. Dewhirst,et al.  Thresholds for thermal damage to normal tissues: An update , 2011, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[21]  T. Dipetrillo,et al.  Combined radiofrequency ablation and high-dose rate brachytherapy for early-stage non-small-cell lung cancer. , 2011, Brachytherapy.

[22]  Nagraj G Huilgol,et al.  Hyperthermia with radiation in the treatment of locally advanced head and neck cancer: a report of randomized trial. , 2010, Journal of cancer research and therapeutics.

[23]  M Zaider,et al.  Cell-survival probability at large doses: an alternative to the linear-quadratic model , 2010, Physics in medicine and biology.

[24]  Zhibin Huang,et al.  A Generalized Linear-Quadratic Model for Radiosurgery, Stereotactic Body Radiation Therapy, and High–Dose Rate Brachytherapy , 2010, Science Translational Medicine.

[25]  Robert J Griffin,et al.  Mild temperature hyperthermia and radiation therapy: Role of tumour vascular thermotolerance and relevant physiological factors , 2010, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[26]  Dieter Haemmerich,et al.  Biophysics of radiofrequency ablation. , 2010, Critical reviews in biomedical engineering.

[27]  Carlos Rinaldi,et al.  Applications of magnetic nanoparticles in medicine: magnetic fluid hyperthermia. , 2009, Puerto Rico health sciences journal.

[28]  Hao-Yu Tseng,et al.  Localised heating of tumours utilising injectable magnetic nanoparticles for hyperthermia cancer therapy. , 2009, IET nanobiotechnology.

[29]  G. Arcangeli,et al.  Hyperthermia as an adjuvant to radiation therapy of recurrent or metastatic malignant melanoma. A multicentre randomized trial by the European Society for Hyperthermic Oncology , 2009, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[30]  Sanyuan Hu,et al.  Microwave ablation with cooled-tip electrode for liver cancer: an analysis of 160 cases. , 2008, Hepato-gastroenterology.

[31]  Lawrence B Marks,et al.  The linear-quadratic model is inappropriate to model high dose per fraction effects in radiosurgery. , 2008, Seminars in radiation oncology.

[32]  M. Astrahan,et al.  Some implications of linear-quadratic-linear radiation dose-response with regard to hypofractionation. , 2008, Medical physics.

[33]  B. Kavanagh,et al.  Toward a unified survival curve: in regard to Park et al. (IntJ Radiat Oncol Biol Phys 2008;70:847-852) and Krueger et al. (Int J Radiat Oncol Biol Phys 2007;69:1262-1271). , 2008, International journal of radiation oncology, biology, physics.

[34]  David J. Carlson,et al.  Combined Use of Monte Carlo DNA Damage Simulations and Deterministic Repair Models to Examine Putative Mechanisms of Cell Killing , 2008, Radiation research.

[35]  Lech Papiez,et al.  Universal survival curve and single fraction equivalent dose: useful tools in understanding potency of ablative radiotherapy. , 2008, International journal of radiation oncology, biology, physics.

[36]  Christer Lindquist,et al.  THE LEKSELL GAMMA KNIFE PERFEXION AND COMPARISONS WITH ITS PREDECESSORS , 2007, Neurosurgery.

[37]  Kim Butts Pauly,et al.  MR thermometry , 2008, Journal of magnetic resonance imaging : JMRI.

[38]  Muneeb Ahmed,et al.  RF ablation with adjuvant therapy: Comparison of external beam radiation and liposomal doxorubicin on ablation efficacy in an animal tumor model , 2008, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[39]  John Y. K. Lee,et al.  Gamma Knife thalamotomy for essential tremor. , 2008, Journal of neurosurgery.

[40]  J. Overgaard,et al.  Hyperthermia: a potent enhancer of radiotherapy. , 2007, Clinical oncology (Royal College of Radiologists (Great Britain)).

[41]  J. Luketich,et al.  Ablative treatments for lung tumors: radiofrequency ablation, stereotactic radiosurgery, and microwave ablation. , 2007, Thoracic surgery clinics.

[42]  Hui-Xiong Xu,et al.  Liver cancer: increased microwave delivery to ablation zone with cooled-shaft antenna--experimental and clinical studies. , 2007, Radiology.

[43]  D. Wilkins,et al.  α/β ratio: A dose range dependence study , 2007 .

[44]  D. Wilkins,et al.  Alpha/beta ratio: A dose range dependence study. , 2007, International journal of radiation oncology, biology, physics.

[45]  M. Hiraoka,et al.  Regional hyperthermia combined with radiotherapy for locally advanced non-small cell lung cancers: a multi-institutional prospective randomized trial of the International Atomic Energy Agency , 2007, International Journal of Clinical Oncology.

[46]  T. Dipetrillo,et al.  Percutaneous image-guided thermal ablation and radiation therapy: outcomes of combined treatment for 41 patients with inoperable stage I/II non-small-cell lung cancer. , 2006, Journal of vascular and interventional radiology : JVIR.

[47]  J. Lepock How do cells respond to their thermal environment? , 2005, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[48]  S. Takashima,et al.  [Results of local ablation therapy for liver metastases from colorectal cancer using radiofrequency ablation and microwave coagulation therapy (RFA/MCT)]. , 2005, Gan to kagaku ryoho. Cancer & chemotherapy.

[49]  Zeljko Vujaskovic,et al.  Randomized trial of hyperthermia and radiation for superficial tumors. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[50]  S. Goldberg,et al.  Reduced tumor growth with combined radiofrequency ablation and radiation therapy in a rat breast tumor model. , 2005, Radiology.

[51]  M. Hiraoka,et al.  Regional hyperthermia combined with radiotherapy for uterine cervical cancers: a multi-institutional prospective randomized trial of the international atomic energy agency. , 2005, International journal of radiation oncology, biology, physics.

[52]  Lech Papiez,et al.  Monte carlo simulation of the Leksell Gamma Knife: II. Effects of heterogeneous versus homogeneous media for stereotactic radiosurgery. , 2004, Physics in medicine and biology.

[53]  X Allen Li,et al.  Extending the linear-quadratic model for large fraction doses pertinent to stereotactic radiotherapy. , 2004, Physics in medicine and biology.

[54]  Alan J. Fenn,et al.  Focused Microwave Phased Array Thermotherapy for Ablation of Early-Stage Breast Cancer: Results of Thermal Dose Escalation , 2004, Annals of Surgical Oncology.

[55]  R. Timmerman,et al.  Extracranial Stereotactic Radioablation Physical Principles , 2003, Acta oncologica.

[56]  Stephanie Frost,et al.  Extracranial stereotactic radioablation: results of a phase I study in medically inoperable stage I non-small cell lung cancer. , 2003, Chest.

[57]  M Tanter,et al.  Experimental demonstration of noninvasive transskull adaptive focusing based on prior computed tomography scans. , 2003, The Journal of the Acoustical Society of America.

[58]  M. Dewhirst,et al.  Carcinogenic effects of hyperthermia , 2003, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[59]  J. Lepock,et al.  Cellular effects of hyperthermia: relevance to the minimum dose for thermal damage , 2003, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[60]  Gregory T. Clement,et al.  A non-invasive method for focusing ultrasound through the human skull. , 2002, Physics in medicine and biology.

[61]  S Sawada,et al.  A randomized clinical trial of radiation therapy versus thermoradiotherapy in stage IIIB cervical carcinoma. , 2001, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[62]  A. Hart,et al.  Comparison of radiotherapy alone with radiotherapy plus hyperthermia in locally advanced pelvic tumours: a prospective, randomised, multicentre trial , 2000, The Lancet.

[63]  R M Henkelman,et al.  Prostate cancer: MR imaging and thermometry during microwave thermal ablation-initial experience. , 2000, Radiology.

[64]  M. Galigniana,et al.  A model for the cytoplasmic trafficking of signalling proteins involving the hsp90-binding immunophilins and p50cdc37. , 1999, Cellular signalling.

[65]  Paul Cornes,et al.  Intraoperative Irradiation: Techniques and Results , 1999 .

[66]  Hiromi Terashima,et al.  Local Control of Nonsmall Cell Lung Cancer by Radiotherapy Combined with High Power Hyperthermia Using an 8MHz RF Capacitive Heating Device. , 1999 .

[67]  Michael C. Kolios,et al.  A theoretical comparison of energy sources--microwave, ultrasound and laser--for interstitial thermal therapy. , 1998, Physics in medicine and biology.

[68]  T L Phillips,et al.  Survival benefit of hyperthermia in a prospective randomized trial of brachytherapy boost +/- hyperthermia for glioblastoma multiforme. , 1998, International journal of radiation oncology, biology, physics.

[69]  C. Song,et al.  Improvement of tumor oxygenation status by mild temperature hyperthermia alone or in combination with carbogen. , 1997, Seminars in oncology.

[70]  P. Liang,et al.  Molecular chaperones and the cytoskeleton. , 1997, Journal of cell science.

[71]  M. Dewhirst,et al.  Combined external beam irradiation and external regional hyperthermia for locally advanced adenocarcinoma of the prostate. , 1997, International journal of radiation oncology, biology, physics.

[72]  D Machin,et al.  Radiotherapy with or without hyperthermia in the treatment of superficial localized breast cancer: results from five randomized controlled trials. International Collaborative Hyperthermia Group. , 1996, International journal of radiation oncology, biology, physics.

[73]  S T Clegg,et al.  Estimation of cell survival in tumours heated to nonuniform temperature distributions. , 1996, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[74]  K Hynynen,et al.  Noninvasive arterial occlusion using MRI-guided focused ultrasound. , 1996, Ultrasound in medicine & biology.

[75]  I. Lax,et al.  Stereotactic high dose fraction radiation therapy of extracranial tumors using an accelerator. Clinical experience of the first thirty-one patients. , 1995, Acta oncologica.

[76]  Raaphorst Gp,et al.  Hyperthermia radiosensitization in human glioma cells comparison of recovery of polymerase activity, survival, and potentially lethal damage repair , 1994 .

[77]  G. Raaphorst,et al.  Hyperthermia radiosensitization in human glioma cells comparison of recovery of polymerase activity, survival, and potentially lethal damage repair. , 1994, International journal of radiation oncology, biology, physics.

[78]  W. Dewey Arrhenius relationships from the molecule and cell to the clinic. , 1994, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[79]  M. Amichetti,et al.  Report of long-term follow-up in a randomized trial comparing radiation therapy and radiation therapy plus hyperthermia to metastatic lymph nodes in stage IV head and neck patients. , 1994, International journal of radiation oncology, biology, physics.

[80]  D. McEachern,et al.  Sensitivity of human cells to mild hyperthermia. , 1993, Cancer research.

[81]  K. Hynynen,et al.  MRI-guided noninvasive ultrasound surgery. , 1993, Medical physics.

[82]  C. Ling,et al.  Moderate hyperthermia and low dose rate irradiation. , 1988, Radiation research.

[83]  J F Fowler,et al.  A review of alpha/beta ratios for experimental tumors: implications for clinical studies of altered fractionation. , 1985, International journal of radiation oncology, biology, physics.

[84]  M. Dewhirst,et al.  The utility of thermal dose as a predictor of tumor and normal tissue responses to combined radiation and hyperthermia. , 1984, Cancer research.

[85]  E. Gillette Clinical use of thermal enhancement and therapeutic gain for hyperthermia combined with radiation or drugs. , 1984, Cancer research.

[86]  W. Dewey,et al.  Hyperthermia — Basic Biology1 , 1984 .

[87]  J J Lagendijk,et al.  A three-dimensional description of heating patterns in vascularised tissues during hyperthermic treatment , 1984, Physics in medicine and biology.

[88]  S. Sapareto,et al.  Differential effect of hyperthermia on murine bone marrow normal colony-forming units and AKR and L1210 leukemia stem cells. , 1984, Cancer research.

[89]  W. Dewey,et al.  Thermal dose determination in cancer therapy. , 1984, International journal of radiation oncology, biology, physics.

[90]  W. Dewey,et al.  Hyperthermia--basic biology. , 1984, Progress in experimental tumor research.

[91]  J. Overgaard,et al.  Formula to estimate the thermal enhancement ratio of a single simultaneous hyperthermia and radiation treatment. , 1984, Acta radiologica. Oncology.

[92]  E. Azzam,et al.  A comparison of cell killing by heat and/or X rays in Chinese hamster V79 cells, Friend erythroleukemia mouse cells, and human thymocyte MOLT-4 cells. , 1983, Radiation research.

[93]  J. Overgaard,et al.  Influence of sequence and interval on the biological response to combined hyperthermia and radiation. , 1982, National Cancer Institute monograph.

[94]  M. Lederman The early history of radiotherapy: 1895-1939. , 1981, International journal of radiation oncology, biology, physics.

[95]  J W Gray,et al.  Effects of hyperthermia on survival and progression of Chinese hamster ovary cells. , 1978, Cancer research.

[96]  W. Dewey,et al.  Cellular responses to combinations of hyperthermia and radiation. , 1977, Radiology.

[97]  R. Humphrey,et al.  The radiation response of human malignant melanoma cells grown in vitro. , 1971, Cancer research.

[98]  W J FRY,et al.  Production of focal destructive lesions in the central nervous system with ultrasound. , 1954, Journal of neurosurgery.

[99]  L. Leksell The stereotaxic method and radiosurgery of the brain. , 1951, Acta chirurgica Scandinavica.