Thermal ablation in non-small cell lung cancer: a review of treatment modalities and the evidence for combination with immune checkpoint inhibitors

Lung cancer is the leading cause of cancer death worldwide, with approximately 1.6 million cancer related deaths each year. Prognosis is best in patients with early stage disease, though even then five-year survival is only 55% in some groups. Median survival for advanced non-small cell lung cancer (NSCLC) is 8–12 months with conventional treatment. Immune checkpoint inhibitor (ICI) therapy has revolutionised the treatment of NSCLC with significant long-term improvements in survival demonstrated in some patients with advanced NSCLC. However, only a small proportion of patients respond to ICI, suggesting the need for further techniques to harness the potential of ICI therapy. Thermal ablation utilizes the extremes of temperature to cause tumour destruction. Commonly used modalities are radiofrequency ablation (RFA), cryoablation and microwave ablation (MWA). At present thermal ablation is reserved for curative-intent therapy in patients with localized NSCLC who are unable to undergo surgical resection or stereotactic ablative body radiotherapy (SABR). Limited evidence suggests that thermal ablative modalities can upregulate an anticancer immune response in NSCLC. It is postulated that thermal ablation can increase tumour antigen release, which would initiate and upregulated steps in the cancer immunity cycle required to elicit an anticancer immune response. This article will review the current thermal ablative techniques and their ability to modulate an anti-cancer immune response with a view of using thermal ablation in conjunction with ICI therapy.

[1]  Daniel P Steinfort,et al.  Emerging and multifaceted role of neutrophils in lung cancer , 2021, Translational lung cancer research.

[2]  K. Sutherland,et al.  Exploring natural killer cell immunology as a therapeutic strategy in lung cancer , 2021, Translational lung cancer research.

[3]  M. Christie,et al.  Bronchoscopic Thermal Vapour Ablation for Localized Cancer Lesions of the Lung: A Clinical Feasibility Treat-and-Resect Study , 2021, Respiration.

[4]  Daniel P Steinfort,et al.  Integrating endobronchial ultrasound bronchoscopy with molecular testing of immunotherapy biomarkers in non-small cell lung cancer , 2020, Translational lung cancer research.

[5]  F. Herth,et al.  Bronchoscopic treatments for early-stage peripheral lung cancer: Are we ready for prime time? , 2020, Respirology.

[6]  A. Valipour,et al.  Bronchial Rheoplasty for Treatment of Chronic Bronchitis. Twelve-Month Results from a Multicenter Clinical Trial , 2020, American journal of respiratory and critical care medicine.

[7]  Nayoung K. D. Kim,et al.  Single-cell RNA sequencing demonstrates the molecular and cellular reprogramming of metastatic lung adenocarcinoma , 2020, Nature Communications.

[8]  L. Otterbein,et al.  Characterization of pulmonary immune responses to hyperoxia by high-dimensional mass cytometry analyses , 2020, Scientific Reports.

[9]  Cryoablation Combined With Camrelizumab and Apatinib for Multiprimary Lung Cancer , 2019, Case Medical Research.

[10]  Fumito Ito,et al.  In situ thermal ablation augments antitumor efficacy of adoptive T cell therapy , 2019, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[11]  Liangrong Shi,et al.  Inflammation induced by incomplete radiofrequency ablation accelerates tumor progression and hinders PD-1 immunotherapy , 2019, Nature Communications.

[12]  Microwave Ablation in Combination With Camrelizumab Versus Camrelizumab in Metastatic Non-small-cell Lung Cancer , 2019, Case Medical Research.

[13]  G. Hanna,et al.  The Abscopal Effect of Stereotactic Radiotherapy and Immunotherapy: Fool's Gold or El Dorado? , 2019, Clinical oncology (Royal College of Radiologists (Great Britain)).

[14]  Sheng-ping Li,et al.  Immunomodulatory Effect after Irreversible Electroporation in Patients with Locally Advanced Pancreatic Cancer , 2019, Journal of oncology.

[15]  Paul Hofman,et al.  Multiplexed Immunohistochemistry for Molecular and Immune Profiling in Lung Cancer—Just About Ready for Prime-Time? , 2019, Cancers.

[16]  Sanjay Gupta,et al.  Irreversible electroporation reverses resistance to immune checkpoint blockade in pancreatic cancer , 2019, Nature Communications.

[17]  Yang Wang,et al.  A Meta-Analysis of Clinical Outcomes After Radiofrequency Ablation and Microwave Ablation for Lung Cancer and Pulmonary Metastases. , 2019, Journal of the American College of Radiology : JACR.

[18]  J. Galon,et al.  Approaches to treat immune hot, altered and cold tumours with combination immunotherapies , 2019, Nature Reviews Drug Discovery.

[19]  S. Leroy,et al.  Current views on tumor mutational burden in patients with non-small cell lung cancer treated by immune checkpoint inhibitors. , 2019, Journal of thoracic disease.

[20]  A. Larson,et al.  Early Immunologic Response of Irreversible Electroporation versus Cryoablation in a Rodent Model of Pancreatic Cancer. , 2018, Journal of vascular and interventional radiology : JVIR.

[21]  E. Yoshida,et al.  Patient and Facility Demographics Related Outcomes in Early-Stage Non-Small Cell Lung Cancer Treated with Radiofrequency Ablation: A National Cancer Database Analysis. , 2018, Journal of vascular and interventional radiology : JVIR.

[22]  A. Chiang,et al.  Survival Rates after Thermal Ablation versus Stereotactic Radiation Therapy for Stage 1 Non-Small Cell Lung Cancer: A National Cancer Database Study. , 2018, Radiology.

[23]  E. Yoshida,et al.  A National Cancer Database Analysis of Radiofrequency Ablation versus Stereotactic Body Radiotherapy in Early-Stage Non-Small Cell Lung Cancer. , 2018, Journal of vascular and interventional radiology : JVIR.

[24]  R. Herbst,et al.  Clinical Features and Management of Acquired Resistance to PD‐1 Axis Inhibitors in 26 Patients With Advanced Non–Small Cell Lung Cancer , 2018, Journal of thoracic oncology : official publication of the International Association for the Study of Lung Cancer.

[25]  Shirley Wu,et al.  Immunological Aspects of Cryoablation of Non-Small Cell Lung Cancer: A Comprehensive Review. , 2018, Journal of thoracic oncology : official publication of the International Association for the Study of Lung Cancer.

[26]  Arnaud Boyer,et al.  Durvalumab after chemoradiotherapy in stage III non-small cell lung cancer. , 2018, Journal of thoracic disease.

[27]  G. Askin,et al.  Clinical Outcomes after Pulmonary Cryoablation with the Use of a Triple Freeze Protocol. , 2018, Journal of vascular and interventional radiology : JVIR.

[28]  C. Drake,et al.  Combining immune check-point blockade and cryoablation in an immunocompetent hormone sensitive murine model of prostate cancer , 2018, Prostate Cancer and Prostatic Diseases.

[29]  Wenbin Zhou,et al.  Enhanced antitumor efficacy through microwave ablation in combination with immune checkpoints blockade in breast cancer: A pre-clinical study in a murine model. , 2018, Diagnostic and interventional imaging.

[30]  X. Jing,et al.  Dynamic changes of T-cell subsets and their relation with tumor recurrence after microwave ablation in patients with hepatocellular carcinoma , 2018, Journal of cancer research and therapeutics.

[31]  L. Niu,et al.  Tumor cryoablation in combination with natural killer cells therapy and Herceptin in patients with HER2‐overexpressing recurrent breast cancer , 2017, Molecular immunology.

[32]  K. Rabe,et al.  Precision Diagnosis and Treatment for Advanced Non-Small-Cell Lung Cancer. , 2017, The New England journal of medicine.

[33]  J. Aerts,et al.  Checkpoint Blockade in Lung Cancer and Mesothelioma , 2017, American journal of respiratory and critical care medicine.

[34]  B. Han,et al.  Navigation Bronchoscopy-Guided Radiofrequency Ablation for Nonsurgical Peripheral Pulmonary Tumors , 2017, Respiration.

[35]  E. Galanis,et al.  Endogenous Heat‐Shock Protein Induction with or Without Radiofrequency Ablation or Cryoablation in Patients with Stage IV Melanoma , 2017, The oncologist.

[36]  H. Takaki,et al.  Thermal ablation and immunomodulation: From preclinical experiments to clinical trials. , 2017, Diagnostic and interventional imaging.

[37]  B. Luo,et al.  Effect of a hypoxic microenvironment after radiofrequency ablation on residual hepatocellular cell migration and invasion , 2017, Cancer science.

[38]  X. Hou,et al.  Effects of microwave ablation on T-cell subsets and cytokines of patients with hepatocellular carcinoma , 2017, Minimally invasive therapy & allied technologies : MITAT : official journal of the Society for Minimally Invasive Therapy.

[39]  I. Mellman,et al.  Elements of cancer immunity and the cancer–immune set point , 2017, Nature.

[40]  Chen Junhui,et al.  Changes of CD4+ T-cell subsets after radiofrequency ablation in lung cancer and its significance. , 2016, Journal of cancer research and therapeutics.

[41]  Y. Igarashi,et al.  Th2 Dominance Might Induce Carcinogenesis in Patients with HCV-related Liver Cirrhosis. , 2016, Anticancer research.

[42]  Janice S. Sung,et al.  A Pilot Study of Preoperative Single-Dose Ipilimumab and/or Cryoablation in Women with Early-Stage Breast Cancer with Comprehensive Immune Profiling , 2016, Clinical Cancer Research.

[43]  A. Enk,et al.  Immune Response After Radiofrequency Ablation and Surgical Resection in Nonsmall Cell Lung Cancer. , 2016, Seminars in thoracic and cardiovascular surgery.

[44]  Yuan Lu,et al.  The Application of Cytidyl Guanosyl Oligodeoxynucleotide Can Affect the Antitumor Immune Response Induced by a Combined Protocol of Cryoablation and Dendritic Cells in Lewis Lung Cancer Model , 2016, Medical science monitor : international medical journal of experimental and clinical research.

[45]  Jingting Jiang,et al.  PD-1 Blockade Boosts Radiofrequency Ablation–Elicited Adaptive Immune Responses against Tumor , 2016, Clinical Cancer Research.

[46]  J. Debus,et al.  A randomized phase II study of radiation induced immune boost in operable non-small cell lung cancer (RadImmune trial) , 2015, BMC Cancer.

[47]  Jason B. Williams,et al.  Commensal Bifidobacterium promotes antitumor immunity and facilitates anti–PD-L1 efficacy , 2015, Science.

[48]  F. Ginhoux,et al.  Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota , 2015, Science.

[49]  Daniel T. Fisher,et al.  Immune Adjuvant Activity of Pre-Resectional Radiofrequency Ablation Protects against Local and Systemic Recurrence in Aggressive Murine Colorectal Cancer , 2015, PloS one.

[50]  T. Atwell,et al.  A national analysis of the complications, cost, and mortality of percutaneous lung ablation. , 2015, Journal of vascular and interventional radiology : JVIR.

[51]  Toshiki Yokoyama,et al.  Bronchoscopy-Guided Cooled Radiofrequency Ablation as a Novel Intervention Therapy for Peripheral Lung Cancer , 2015, Respiration.

[52]  E. Bonifacio,et al.  Widespread seasonal gene expression reveals annual differences in human immunity and physiology , 2015, Nature Communications.

[53]  Shizhong Zhang,et al.  Synergism between cryoablation and GM-CSF: enhanced immune function of splenic dendritic cells in mice with glioma , 2015, Neuroreport.

[54]  Wendy S. Garrett,et al.  Cancer and the microbiota , 2015, Science.

[55]  Ronak Talati,et al.  Five-year survival after cryoablation of stage I non-small cell lung cancer in medically inoperable patients. , 2015, Journal of vascular and interventional radiology : JVIR.

[56]  T. de Baère,et al.  Radiofrequency ablation is a valid treatment option for lung metastases: experience in 566 patients with 1037 metastases , 2015, Annals of oncology : official journal of the European Society for Medical Oncology.

[57]  T. Baère,et al.  Irreversible Electroporation (IRE) Fails to Demonstrate Efficacy in a Prospective Multicenter Phase II Trial on Lung Malignancies: The ALICE Trial , 2015, CardioVascular and Interventional Radiology.

[58]  J. G. Lee,et al.  Tumor-Specific Immunity Induced by Cryoablation in a Murine Renal Cell Carcinoma Model , 2014, Korean journal of urology.

[59]  H. Kohrt,et al.  Predictive correlates of response to the anti-PD-L1 antibody MPDL3280A in cancer patients , 2014, Nature.

[60]  Shizhong Zhang,et al.  In-situ administration of dendritic cells following argon–helium cryosurgery enhances specific antiglioma immunity in mice , 2014, Neuroreport.

[61]  Shizhong Zhang,et al.  Antitumor efficacy of argon–helium cryoablation-generated dendritic cell vaccine in glioma , 2014, Neuroreport.

[62]  B. Meyers,et al.  Patterns of survival and recurrence after surgical treatment of early stage non-small cell lung carcinoma in the ACOSOG Z0030 (ALLIANCE) trial. , 2014, The Journal of thoracic and cardiovascular surgery.

[63]  J. Kettenbach,et al.  Radiofrequency ablation suppresses distant tumour growth in a novel rat model of multifocal hepatocellular carcinoma. , 2014, Clinical science.

[64]  Daniel T. Fisher,et al.  The two faces of IL-6 in the tumor microenvironment. , 2014, Seminars in immunology.

[65]  E. Vadai,et al.  Cryoimmunotherapy with local co-administration of ex vivo generated dendritic cells and CpG-ODN immune adjuvant, elicits a specific antitumor immunity , 2014, Cancer Immunology, Immunotherapy.

[66]  S. Kaneko,et al.  In vivo immunological antitumor effect of OK-432-stimulated dendritic cell transfer after radiofrequency ablation , 2014, Cancer Immunology, Immunotherapy.

[67]  F. Marincola,et al.  Commensal Bacteria Control Cancer Response to Therapy by Modulating the Tumor Microenvironment , 2013, Science.

[68]  Eric Vivier,et al.  The Intestinal Microbiota Modulates the Anticancer Immune Effects of Cyclophosphamide , 2013, Science.

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

[70]  W. Xiaohua,et al.  Therapeutic outcomes of combining cryotherapy, chemotherapy and DC-CIK immunotherapy in the treatment of metastatic non-small cell lung cancer. , 2013, Cryobiology.

[71]  D. de Ruysscher,et al.  Early and locally advanced non-small-cell lung cancer (NSCLC): ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. , 2013, Annals of oncology : official journal of the European Society for Medical Oncology.

[72]  M. Yasuo,et al.  Clinical Experience of Bronchoscopy-Guided Radiofrequency Ablation for Peripheral-Type Lung Cancer , 2013, Case reports in oncological medicine.

[73]  M. Gonen,et al.  Image-guided thermal ablation of tumors increases the plasma level of interleukin-6 and interleukin-10. , 2013, Journal of vascular and interventional radiology : JVIR.

[74]  I. Mellman,et al.  Oncology meets immunology: the cancer-immunity cycle. , 2013, Immunity.

[75]  T. Si,et al.  Analysis of circulating regulatory T cells (CD4+CD25+CD127-) after cryosurgery in prostate cancer. , 2013, Asian journal of andrology.

[76]  L. Niu,et al.  Combination treatment with comprehensive cryoablation and immunotherapy in metastatic hepatocellular cancer. , 2013, World journal of gastroenterology.

[77]  Jonathan D. Stallings,et al.  Improved Local and Systemic Anti-Tumor Efficacy for Irreversible Electroporation in Immunocompetent versus Immunodeficient Mice , 2013, PloS one.

[78]  A. Yamamoto,et al.  Radiofrequency ablation and immunostimulant OK-432: combination therapy enhances systemic antitumor immunity for treatment of VX2 lung tumors in rabbits. , 2013, Radiology.

[79]  A. Chang,et al.  Treatment of stage I and II non-small cell lung cancer: Diagnosis and management of lung cancer, 3rd ed: American College of Chest Physicians evidence-based clinical practice guidelines. , 2013, Chest.

[80]  T. Kagaya,et al.  Enhancement of tumor‐associated antigen‐specific T cell responses by radiofrequency ablation of hepatocellular carcinoma , 2013, Hepatology.

[81]  Zhao Li,et al.  Immunologic Response to Tumor Ablation with Irreversible Electroporation , 2012, PloS one.

[82]  J. Bosch,et al.  Radio frequency ablation combined with interleukin-2 induces an antitumor immune response to renal cell carcinoma in a murine model. , 2012, The Journal of urology.

[83]  David C. Smith,et al.  Safety, activity, and immune correlates of anti-PD-1 antibody in cancer. , 2012, The New England journal of medicine.

[84]  Daniel P Steinfort,et al.  Comparative effectiveness of radial probe endobronchial ultrasound versus CT-guided needle biopsy for evaluation of peripheral pulmonary lesions: a randomized pragmatic trial. , 2011, Respiratory medicine.

[85]  J. Furuse,et al.  Radiofrequency ablation for hepatocellular carcinoma induces glypican-3 peptide-specific cytotoxic T lymphocytes. , 2011, International journal of oncology.

[86]  A. Thakur,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 , 2011, Journal of immunotherapy.

[87]  H. Rammensee,et al.  Analysis of tumor antigen‐specific T cells and antibodies in cancer patients treated with radiofrequency ablation , 2011, International journal of cancer.

[88]  Damian E. Dupuy,et al.  Irreversible Electroporation in a Swine Lung Model , 2011, CardioVascular and Interventional Radiology.

[89]  R. Schreiber,et al.  Cancer Immunoediting: Integrating Immunity’s Roles in Cancer Suppression and Promotion , 2011, Science.

[90]  D. Hanahan,et al.  Hallmarks of Cancer: The Next Generation , 2011, Cell.

[91]  Boris Rubinsky,et al.  Irreversible electroporation near the heart: ventricular arrhythmias can be prevented with ECG synchronization. , 2011, AJR. American journal of roentgenology.

[92]  G. Gravante,et al.  Changes in interleukin-1β and 6 after hepatic microwave tissue ablation compared with radiofrequency, cryotherapy and surgical resections. , 2010, American journal of surgery.

[93]  D. Schadendorf,et al.  Improved survival with ipilimumab in patients with metastatic melanoma. , 2010, The New England journal of medicine.

[94]  A. Yamamoto,et al.  Determinants of Local Progression After Computed Tomography-Guided Percutaneous Radiofrequency Ablation for Unresectable Lung Tumors: 9-Year Experience in a Single Institution , 2010, CardioVascular and Interventional Radiology.

[95]  C. Georgiades,et al.  Radiofrequency ablation: mechanism of action and devices. , 2010, Journal of vascular and interventional radiology : JVIR.

[96]  Christopher L Brace,et al.  Microwave tumor ablation: mechanism of action, clinical results, and devices. , 2010, Journal of vascular and interventional radiology : JVIR.

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

[98]  Jun‐liang Fu,et al.  Regulatory T cells are associated with post-cryoablation prognosis in patients with hepatitis B virus-related hepatocellular carcinoma , 2010, Journal of Gastroenterology.

[99]  T. Si,et al.  [Effect of transcatheter renal arterial embolization combined with cryoablation on regulatory CD4+ CD25+ T lymphocytes in the peripheral blood of patients with advanced renal carcinoma]. , 2010, Zhonghua yi xue za zhi.

[100]  S. Rossi,et al.  Systemic inflammatory response and downmodulation of peripheral CD25+Foxp3+ T-regulatory cells in patients undergoing radiofrequency thermal ablation for lung cancer. , 2009, Human immunology.

[101]  P. V. van Diest,et al.  Accelerated Perinecrotic Outgrowth of Colorectal Liver Metastases Following Radiofrequency Ablation is a Hypoxia-Driven Phenomenon , 2009, Annals of surgery.

[102]  P. Allavena,et al.  Tumor-associated macrophages and the related myeloid-derived suppressor cells as a paradigm of the diversity of macrophage activation. , 2009, Human immunology.

[103]  H. Bear,et al.  Radiofrequency thermal ablation of breast tumors combined with intralesional administration of IL-7 and IL-15 augments anti-tumor immune responses and inhibits tumor development and metastasis , 2009, Breast Cancer Research and Treatment.

[104]  X. Hao,et al.  Combined Cryoablation and GM-CSF Treatment for Metastatic Hormone Refractory Prostate Cancer , 2009, Journal of immunotherapy.

[105]  X. Hao,et al.  Immunologic response to primary cryoablation of high-risk prostate cancer. , 2008, Cryobiology.

[106]  Carlo Bartolozzi,et al.  Response to radiofrequency ablation of pulmonary tumours: a prospective, intention-to-treat, multicentre clinical trial (the RAPTURE study). , 2008, The Lancet. Oncology.

[107]  William R. Lees,et al.  Radiofrequency ablation of lung metastases: factors influencing success , 2008, European Radiology.

[108]  K. Elkon,et al.  Innate and adaptive immune response to apoptotic cells. , 2007, Journal of autoimmunity.

[109]  K. Kubo,et al.  Bronchoscopy-guided radiofrequency ablation as a potential novel therapeutic tool , 2007, European Respiratory Journal.

[110]  William W Mayo-Smith,et al.  Pulmonary radiofrequency ablation: long-term safety and efficacy in 153 patients. , 2007, Radiology.

[111]  R. Siegel,et al.  Autoimmunity versus tolerance: can dying cells tip the balance? , 2007, Clinical immunology.

[112]  Takao Hiraki,et al.  Risk factors for local progression after percutaneous radiofrequency ablation of lung tumors , 2006, Cancer.

[113]  Z. Trajanoski,et al.  Type, Density, and Location of Immune Cells Within Human Colorectal Tumors Predict Clinical Outcome , 2006, Science.

[114]  A. Ravaud,et al.  Midterm local efficacy and survival after radiofrequency ablation of lung tumors with minimum follow-up of 1 year: prospective evaluation. , 2006, Radiology.

[115]  C. Figdor,et al.  Synergy between in situ cryoablation and TLR9 stimulation results in a highly effective in vivo dendritic cell vaccine. , 2006, Cancer research.

[116]  E. Berber,et al.  Pattern of carcinoembryonic antigen drop after laparoscopic radiofrequency ablation of liver metastasis from colorectal carcinoma , 2006, Cancer.

[117]  D. Schuppan,et al.  Activation and dramatically increased cytolytic activity of tumor specific T lymphocytes after radio-frequency ablation in patients with hepatocellular carcinoma and colorectal liver metastases. , 2006, World journal of gastroenterology.

[118]  C. Akdis,et al.  Mechanisms of immune suppression by interleukin‐10 and transforming growth factor‐β: the role of T regulatory cells , 2006, Immunology.

[119]  G. Missale,et al.  Radiofrequency thermal ablation of hepatocellular carcinoma liver nodules can activate and enhance tumor-specific T-cell responses. , 2006, Cancer research.

[120]  B. Tirosh,et al.  Combined Dendritic Cell Cryotherapy of Tumor Induces Systemic Antimetastatic Immunity , 2005, Clinical Cancer Research.

[121]  K. Saijo,et al.  Microwave tumour coagulation plus in situ treatment with cytokine-microparticles: Induction of potent anti-residual tumour immunity , 2005, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[122]  K. Knutson,et al.  Tumor antigen-specific T helper cells in cancer immunity and immunotherapy , 2005, Cancer Immunology, Immunotherapy.

[123]  S. Fu,et al.  TGF‐β Induces Foxp3 + T‐Regulatory Cells from CD4 + CD25 − Precursors , 2004, American journal of transplantation : official journal of the American Society of Transplantation and the American Society of Transplant Surgeons.

[124]  Carl G. Figdor,et al.  In Situ Tumor Ablation Creates an Antigen Source for the Generation of Antitumor Immunity , 2004, Cancer Research.

[125]  P. Liang,et al.  Significance of changes in local immunity in patients with hepatocellular carcinoma after percutaneous microwave coagulation therapy. , 2002, Chinese medical journal.

[126]  R. Vile Faculty Opinions recommendation of IFNgamma and lymphocytes prevent primary tumour development and shape tumour immunogenicity. , 2001 .

[127]  J. Banchereau,et al.  IL-6 switches the differentiation of monocytes from dendritic cells to macrophages , 2000, Nature Immunology.

[128]  H. Band,et al.  Hsp72-mediated augmentation of MHC class I surface expression and endogenous antigen presentation. , 1998, International immunology.

[129]  F. Pecchio,et al.  [Evaluation of some nonspecific immunological parameters in patients with oral cavity carcinoma undergoing cryosurgery]. , 1980, Bollettino della Societa italiana di biologia sperimentale.

[130]  Jie Xu,et al.  Molecular and Cellular Functions of CTLA-4. , 2020, Advances in experimental medicine and biology.

[131]  Jie Xu Regulation of Cancer Immune Checkpoints: Molecular and Cellular Mechanisms and Therapy , 2020 .

[132]  T. Si,et al.  Immunological response induced by cryoablation against murine H22 hepatoma cell line in vivo. , 2018, Cryobiology.

[133]  A. Sidana Cancer immunotherapy using tumor cryoablation. , 2014, Immunotherapy.

[134]  Z. Guo,et al.  Anti-tumor immunological response induced by cryoablation and anti-CTLA-4 antibody in an in vivo RM-1 cell prostate cancer murine model. , 2014, Neoplasma.

[135]  S. Osada,et al.  Growth inhibition of unresectable tumors induced by hepatic cryoablation: report of two cases. , 2008, Hepato-gastroenterology.

[136]  A. Zisman,et al.  PSA elevation during prostate cryosurgery and subsequent decline. , 2005, Urologic oncology.

[137]  P. Srivastava,et al.  Interaction of heat shock proteins with peptides and antigen presenting cells: chaperoning of the innate and adaptive immune responses. , 2002, Annual review of immunology.

[138]  I. Petersen,et al.  [Immunomodulation by cryosurgery in malignant melanoma]. , 1989, Onkologie.

[139]  P. Guinan,et al.  Evaluation of cellular immunologic responsiveness in the clinical management of patients with prostatic cancer. II. Effect of oestrogen, cryosurgery and transurethral resection on thymic-dependent lymphocytic blastogenesis. , 1976, Urologia internationalis.

[140]  Pyt Goh,et al.  Biij Biomedical Imaging and Intervention Journal Radiofrequency Ablation of Lung Tumours , 2022 .