The intersection between immunotherapy and laser interstitial thermal therapy: a multipronged future of neuro-oncology

References

• Bettag M, Ulrich F, Schober R, et al. Stereotactic laser therapy in cerebral gliomas. Acta Neurochir Suppl. 1991;52:81–83.
   PubMedGoogle Scholar
• Sugiyama K, Sakai T, Fujishima I, et al. Stereotactic interstitial laser-hyperthermia using Nd-YAG laser. Stereotact Funct Neurosurg. 1990;54-55:501–505.
   PubMed Web of Science ®Google Scholar
• Banerjee C, Snelling B, Berger MH, et al. The role of magnetic resonance-guided laser ablation in neurooncology. Br J Neurosurg. 2015;29(2):192–196.
   PubMed Web of Science ®Google Scholar
• Prince E, Hakimian S, Ko AL, et al. Laser interstitial thermal therapy for epilepsy. Curr Neurol Neurosci Rep. 2017;17(9):63.
   PubMed Web of Science ®Google Scholar
• Silva D, Sharma M, Juthani R, et al. Magnetic resonance thermometry and laser interstitial thermal therapy for brain tumors. Neurosurg Clin N Am. 2017;28(4):525–533.
   PubMed Web of Science ®Google Scholar
• Ashraf O, Patel NV, Hanft S, et al. Laser-induced thermal therapy in neuro-oncology: a review. World Neurosurg. 2018;112:166–177.
   PubMed Web of Science ®Google Scholar
• Anzai Y, Lufkin RB, Hirschowitz S, et al. MR imaging-histopathologic correlation of thermal injuries induced with interstitial Nd:YAG laser irradiation in the chronic model. J Magn Reson Imaging. 1992;2(6):671–678.
   PubMed Web of Science ®Google Scholar
• Schwarzmaier H-J, Eickmeyer F, von Tempelhoff W, et al. MR-guided laser-induced interstitial thermotherapy of recurrent glioblastoma multiforme: preliminary results in 16 patients. Eur J Radiol. 2006;59(2):208–215.
   PubMed Web of Science ®Google Scholar
• Kahn T, Bettag M, Ulrich F, et al. MRI-guided laser-induced interstitial thermotherapy of cerebral neoplasms. J Comput Assist Tomogr. 1994;18(4):519–532.
   PubMed Web of Science ®Google Scholar
• Reimer P, Bremer C, Horch C, et al. MR-monitored LITT as a palliative concept in patients with high grade gliomas: preliminary clinical experience. J Magn Reson Imaging. 1998;8(1):240–244.
   PubMed Web of Science ®Google Scholar
• Jethwa PR, Barrese JC, Gowda A, et al. Magnetic resonance thermometry-guided laser-induced thermal therapy for intracranial neoplasms: initial experience. Neurosurgery. 2012;71(1 Suppl Operative):133–144.
   PubMed Web of Science ®Google Scholar
• Ahrar K, Gowda A, Javadi S, et al. Preclinical assessment of a 980-nm diode laser ablation system in a large animal tumor model. J Vasc Interv Radiol. 2010;21(4):555–561.
   PubMed Web of Science ®Google Scholar
• Jethwa PR, Barrese JC, Gowda A, et al. Magnetic resonance thermometry-guided laser-induced thermal therapy for intracranial neoplasms: initial experience. Oper Neurosurg. 2012;71(1 Suppl Operative):133–ons45.
   PubMed Web of Science ®Google Scholar
• Sloan AE, Ahluwalia MS, Valerio-Pascua J, et al. Results of the neuroblate system first-in-humans phase I clinical trial for recurrent glioblastoma. J Neurosurg. 2013;118(6):1202–1219.
   PubMed Web of Science ®Google Scholar
• Diaz R, Ivan ME, Hanft S, et al. Laser interstitial thermal therapy: lighting the way to a new treatment option in neurosurgery. Neurosurgery. 2016;79(suppl_1):S3–s7.
   PubMed Web of Science ®Google Scholar
• Norred S, Johnson J. Magnetic resonance-guided laser induced thermal therapy for glioblastoma multiforme: a review. Biomed Res Int. 2014;2014:761312.
   PubMed Web of Science ®Google Scholar
• Rodriguez A, Tatter SB. Laser ablation of recurrent malignant gliomas: current status and future perspective. Neurosurgery. 2016;79(suppl_1):S35–s9.
   PubMed Web of Science ®Google Scholar
• Salem U, Kumar VA, Madewell JE, et al. Neurosurgical applications of MRI guided laser interstitial thermal therapy (LITT). Cancer Imaging. 2019;19(1):65.
   PubMed Web of Science ®Google Scholar
• Stafford R, Fuentes D, Elliott A, et al. Laser-induced thermal therapy for tumor ablation. Crit Rev Biomed Eng. 2010;38(1):79–100.
   PubMedGoogle Scholar
• Patel NV, Mian M, Stafford RJ, et al. Laser interstitial thermal therapy technology, physics of magnetic resonance imaging thermometry, and technical considerations for proper catheter placement during magnetic resonance imaging-guided laser interstitial thermal therapy. Neurosurgery. 2016;79(suppl_1):S8–s16.
   PubMed Web of Science ®Google Scholar
• Rieke V, Butts Pauly K. MR thermometry. J Magn Reson Imaging. 2008;27(2):376–390.
   PubMed Web of Science ®Google Scholar
• Chang IA. Considerations for thermal injury analysis for RF ablation devices. Open Biomed Eng J. 2010;4:3–12.
   PubMedGoogle Scholar
• McNichols RJ, Gowda A, Kangasniemi M, et al. MR thermometry-based feedback control of laser interstitial thermal therapy at 980 nm. Lasers Surg Med. 2004;34(1):48–55.
   PubMed Web of Science ®Google Scholar
• Dewhirst MW, Viglianti BL, Lora-Michiels M, et al. Basic principles of thermal dosimetry and thermal thresholds for tissue damage from hyperthermia. Int J Hyperthermia. 2003;19(3):267–294.
   PubMed Web of Science ®Google Scholar
• Bastos D, Rao G, Oliva ICG, et al. Predictors of local control of brain metastasis treated with laser interstitial thermal therapy. Neurosurgery. 2019 DOI:10.1093/neuros/nyz357.
   Web of Science ®Google Scholar
• Carpentier A, Chauvet D, Reina V, et al. MR-guided laser-induced thermal therapy (LITT) for recurrent glioblastomas. Lasers Surg Med. 2012;44(5):361–368.
   PubMed Web of Science ®Google Scholar
• Carpentier A, McNichols RJ, Stafford RJ, et al. Laser thermal therapy: real-time MRI-guided and computer-controlled procedures for metastatic brain tumors. Lasers Surg Med. 2011;43(10):943–950.
   PubMed Web of Science ®Google Scholar
• Carpentier A, McNichols RJ, Stafford RJ, et al. Real-time magnetic resonance-guided laser thermal therapy for focal metastatic brain tumors. Neurosurgery. 2008;63(1 Suppl 1):ONS21–8; discussion ONS8-9.
   PubMed Web of Science ®Google Scholar
• Drane DL, Loring DW, Voets NL, et al. Better object recognition and naming outcome with MRI-guided stereotactic laser amygdalohippocampotomy for temporal lobe epilepsy. Epilepsia. 2015;56(1):101–113.
   PubMed Web of Science ®Google Scholar
• Kang JY, Wu C, Tracy J, et al. Laser interstitial thermal therapy for medically intractable mesial temporal lobe epilepsy. Epilepsia. 2016;57(2):325–334.
   PubMed Web of Science ®Google Scholar
• Rao MS, Hargreaves EL, Khan AJ, et al. Magnetic resonance-guided laser ablation improves local control for postradiosurgery recurrence and/or radiation necrosis. Neurosurgery. 2014;74(6):658–667; discussion 67.
   PubMed Web of Science ®Google Scholar
• Tatsui CE, Lee SH, Amini B, et al. Spinal laser interstitial thermal therapy: a novel alternative to surgery for metastatic epidural spinal cord compression. Neurosurgery. 2016;79(suppl_1):S73–S82.
   PubMed Web of Science ®Google Scholar
• Thomas JG, Al-Holou WN, de Almeida Bastos DC, et al. A novel use of the intraoperative MRI for metastatic spine tumors: laser interstitial thermal therapy for percutaneous treatment of epidural metastatic spine disease. Neurosurg Clin N Am. 2017;28(4):513–524.
   PubMed Web of Science ®Google Scholar
• Willie JT, Laxpati NG, Drane DL, et al. Real-time magnetic resonance-guided stereotactic laser amygdalohippocampotomy for mesial temporal lobe epilepsy. Neurosurgery. 2014;74(6):569–584; discussion 84-5.
   PubMed Web of Science ®Google Scholar
• Ahluwalia M, Barnett GH, Deng D, et al. Laser ablation after stereotactic radiosurgery: a multicenter prospective study in patients with metastatic brain tumors and radiation necrosis. J Neurosurg. 2018;130(3):804–811.
   PubMed Web of Science ®Google Scholar
• Beaumont TL, Mohammadi AM, Kim AH, et al. Magnetic resonance imaging-guided laser interstitial thermal therapy for glioblastoma of the corpus callosum. Neurosurgery. 2018;83(3):556–565.
   PubMed Web of Science ®Google Scholar
• Borghei-Razavi H, Koech H, Sharma M, et al. Laser interstitial thermal therapy for posterior fossa lesions: an initial experience. World Neurosurg. 2018;117:e146–e53.
   PubMed Web of Science ®Google Scholar
• Chaunzwa TL, Deng D, Leuthardt EC, et al. Laser thermal ablation for metastases failing radiosurgery: a multicentered retrospective study. Neurosurgery. 2018;82(1):56–63.
   PubMed Web of Science ®Google Scholar
• Hale AT, Sen S, Haider AS, et al. Open resection versus laser interstitial thermal therapy for the treatment of pediatric insular epilepsy. Neurosurgery. 2019;85(4):E730–e6.
   PubMed Web of Science ®Google Scholar
• Hernandez RN, Carminucci A, Patel P, et al. Magnetic resonance-guided laser-induced thermal therapy for the treatment of progressive enhancing inflammatory reactions following stereotactic radiosurgery, or PEIRs, for metastatic brain disease. Neurosurgery. 2019;85(1):84–90.
   PubMed Web of Science ®Google Scholar
• Kamath AA, Friedman DD, Akbari SHA, et al. Glioblastoma treated with magnetic resonance imaging-guided laser interstitial thermal therapy: safety, efficacy, and outcomes. Neurosurgery. 2019;84(4):836–843.
   PubMed Web of Science ®Google Scholar
• Morris SA, Rollo M, Rollo P, et al. Prolonged blood-brain barrier disruption following laser interstitial ablation in epilepsy: a case series with a case report of postablation optic neuritis. World Neurosurg. 2017;104:467–475.
   PubMed Web of Science ®Google Scholar
• Palma AE, Wicks RT, Popli G, et al. Corpus callosotomy via laser interstitial thermal therapy: a case series. J Neurosurg Pediatr. 2018;23(3):303–307.
   PubMed Web of Science ®Google Scholar
• Patel P, Patel NV, Danish SF. Intracranial MR-guided laser-induced thermal therapy: single-center experience with the Visualase thermal therapy system. J Neurosurg. 2016;125(4):853–860.
   PubMed Web of Science ®Google Scholar
• Rennert RC, Khan U, Tatter SB, et al. Patterns of clinical use of stereotactic laser ablation: analysis of a Multicenter Prospective Registry. World Neurosurg. 2018;116:e566–e70.
   PubMed Web of Science ®Google Scholar
• Smith CJ, Myers CS, Chapple KM, et al. Long-term follow-up of 25 cases of biopsy-proven radiation necrosis or post-radiation treatment effect treated with magnetic resonance-guided laser interstitial thermal therapy. Neurosurgery. 2016;79(suppl_1):S59–s72.
   PubMed Web of Science ®Google Scholar
• Sun XR, Patel NV, Danish SF. Tissue ablation dynamics during magnetic resonance-guided, laser-induced thermal therapy. Neurosurgery. 2015;77(1):51–58. discussion 8.
   PubMed Web of Science ®Google Scholar
• Tovar-Spinoza Z, Choi H. Magnetic resonance-guided laser interstitial thermal therapy: report of a series of pediatric brain tumors. J Neurosurg Pediatr. 2016;17(6):723–733.
   PubMed Web of Science ®Google Scholar
• Traylor JI, Patel R, Habib A, et al. Laser interstitial thermal therapy to the posterior fossa: challenges and nuances. World Neurosurg. 2019;132:e124–e32.
   PubMed Web of Science ®Google Scholar
• Stupp R, Mason WP, van den Bent MJ, et al.; National Cancer Institute of Canada Clinical Trials Group. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med. 2005;352(10):987–996.
   PubMed Web of Science ®Google Scholar
• Gilbert MR, Dignam JJ, Armstrong TS, et al. A randomized trial of bevacizumab for newly diagnosed glioblastoma. N Engl J Med. 2014;370(8):699–708.
   PubMed Web of Science ®Google Scholar
• Hegi ME, Diserens AC, Gorlia T, et al. MGMT gene silencing and benefit from temozolomide in glioblastoma. N Engl J Med. 2005;352(10):997–1003.
   PubMed Web of Science ®Google Scholar
• Sampson JH, Gunn MD, Fecci PE, et al. Brain immunology and immunotherapy in brain tumours. Nat Rev Cancer. 2020;20(1):12–25.
   PubMed Web of Science ®Google Scholar
• Stummer W, Pichlmeier U, Meinel T, et al.; ALA-Glioma Study Group. Fluorescence-guided surgery with 5-aminolevulinic acid for resection of malignant glioma: a randomised controlled multicentre phase III trial. Lancet Oncol. 2006;7(5):392–401.
   PubMed Web of Science ®Google Scholar
• Stupp R, Taillibert S, Kanner A, et al. Effect of tumor-treating fields plus maintenance temozolomide vs maintenance temozolomide alone on survival in patients with glioblastoma: a randomized clinical trial. JAMA. 2017;318(23):2306–2316.
   PubMed Web of Science ®Google Scholar
• Woroniecka KI, Rhodin KE, Chongsathidkiet P, et al. T-cell dysfunction in glioblastoma: applying a new framework. Clin Cancer Res. 2018;24(16):3792–3802.
   PubMed Web of Science ®Google Scholar
• Barnett GH, Voigt JD, Alhuwalia MS. A systematic review and meta-analysis of studies examining the use of brain laser interstitial thermal therapy versus craniotomy for the treatment of high-grade tumors in or near areas of eloquence: an examination of the extent of resection and major complication rates associated with each type of surgery. Stereotact Funct Neurosurg. 2016;94(3):164–173.
   PubMed Web of Science ®Google Scholar
• Alattar AA, Bartek J, Jr., Chiang VL, et al. Stereotactic laser ablation as treatment of brain metastases recurring after stereotactic radiosurgery: a systematic literature review. World Neurosurg. 2019;128:134–142.
   PubMed Web of Science ®Google Scholar
• Ivan ME, Mohammadi AM, De Deugd N, et al. Laser ablation of newly diagnosed malignant gliomas: a meta-analysis. Neurosurgery. 2016;79(suppl_1):S17–s23.
   PubMed Web of Science ®Google Scholar
• Missios S, Bekelis K, Barnett GH. Renaissance of laser interstitial thermal ablation. Neurosurg Focus. 2015;38(3):E13.
   PubMed Web of Science ®Google Scholar
• Schober R, Bettag M, Sabel M, et al. Fine structure of zonal changes in experimental Nd:YAG laser-induced interstitial hyperthermia. Lasers Surg Med. 1993;13(2):234–241.
   PubMed Web of Science ®Google Scholar
• Tracz RA, Wyman DR, Little PB, et al. Comparison of magnetic resonance images and the histopathological findings of lesions induced by interstitial laser photocoagulation in the brain. Lasers Surg Med. 1993;13(1):45–54.
   PubMed Web of Science ®Google Scholar
• Elder JB, Huntoon K, Otero J, et al. Histologic findings associated with laser interstitial thermotherapy for glioblastoma multiforme. Diagn Pathol. 2019;14(1):19.
   PubMed Web of Science ®Google Scholar
• Patel PD, Patel NV, Davidson C, et al. The role of MRgLITT in overcoming the challenges in managing infield recurrence after radiation for brain metastasis. Neurosurgery. 2016;79(suppl_1):S40–S58.
   PubMed Web of Science ®Google Scholar
• Evans SS, Repasky EA, Fisher DT. Fever and the thermal regulation of immunity: the immune system feels the heat. Nat Rev Immunol. 2015;15(6):335–349.
   PubMed Web of Science ®Google Scholar
• Frey B, Weiss E-M, Rubner Y, et al. Old and new facts about hyperthermia-induced modulations of the immune system. Int J Hyperthermia. 2012;28(6):528–542.
   PubMed Web of Science ®Google Scholar
• Giuliano JS, Jr., Lahni PM, Wong HR, et al. Pediatric sepsis – part V: extracellular heat shock proteins: alarmins for the host immune system. Open Inflamm J. 2011;4:49–60.
   PubMedGoogle Scholar
• Guo D, Chen Y, Wang S, et al. Exosomes from heat-stressed tumour cells inhibit tumour growth by converting regulatory T cells to Th17 cells via IL-6. Immunology. 2018;154(1):132–143.
   PubMed Web of Science ®Google Scholar
• Hatzfeld-Charbonnier AS, Lasek A, Castera L, et al. Influence of heat stress on human monocyte-derived dendritic cell functions with immunotherapeutic potential for antitumor vaccines. J Leukoc Biol. 2007;81(5):1179–1187.
   PubMed Web of Science ®Google Scholar
• Ito A, Fujioka M, Tanaka K, et al. Screening of cytokines to enhance vaccine effects of heat shock protein 70-rich tumor cell lysate. J Biosci Bioeng. 2005;100(1):36–42.
   PubMed Web of Science ®Google Scholar
• Jaattela M. Heat shock proteins as cellular lifeguards. Ann Med. 1999;31(4):261–271.
   PubMed Web of Science ®Google Scholar
• Mace TA, Zhong L, Kokolus KM, et al. Effector CD8+ T cell IFN-γ production and cytotoxicity are enhanced by mild hyperthermia. Int J Hyperthermia. 2012;28(1):9–18.
   PubMed Web of Science ®Google Scholar
• Murshid A, Gong J, Calderwood SK. The role of heat shock proteins in antigen cross presentation. Front Immunol. 2012;3:63.
   PubMed Web of Science ®Google Scholar
• Nikfarjam M, Muralidharan V, Su K, et al. Patterns of heat shock protein (HSP70) expression and Kupffer cell activity following thermal ablation of liver and colorectal liver metastases. Int J Hyperthermia. 2005;21(4):319–332.
   PubMed Web of Science ®Google Scholar
• Ostberg JR, Dayanc BE, Yuan M, et al. Enhancement of natural killer (NK) cell cytotoxicity by fever-range thermal stress is dependent on NKG2D function and is associated with plasma membrane NKG2D clustering and increased expression of MICA on target cells. J Leukoc Biol. 2007;82(5):1322–1331.
   PubMed Web of Science ®Google Scholar
• Ostberg JR, Repasky EA. Emerging evidence indicates that physiologically relevant thermal stress regulates dendritic cell function. Cancer Immunol Immunother. 2006;55(3):292–298.
   PubMed Web of Science ®Google Scholar
• Suzue K, Zhou X, Eisen HN, et al. Heat shock fusion proteins as vehicles for antigen delivery into the major histocompatibility complex class I presentation pathway. Proc Natl Acad Sci USA. 1997;94(24):13146–13151.
   PubMed Web of Science ®Google Scholar
• Toraya-Brown S, Fiering S. Local tumour hyperthermia as immunotherapy for metastatic cancer. Int J Hyperthermia. 2014;30(8):531–539.
   PubMed Web of Science ®Google Scholar
• Toraya-Brown S, Sheen MR, Zhang P, et al. Local hyperthermia treatment of tumors induces CD8+ T cell-mediated resistance against distal and secondary tumors. Nanomedicine 2014;10:1273–1285.
   PubMed Web of Science ®Google Scholar
• Tournier JN, Hellmann AQ, Lesca G, et al. Fever-like thermal conditions regulate the activation of maturing dendritic cells. J Leukoc Biol. 2003;73(4):493–501.
   PubMed Web of Science ®Google Scholar
• Udono H, Levey DL, Srivastava PK. Cellular requirements for tumor-specific immunity elicited by heat shock proteins: tumor rejection antigen gp96 primes CD8+ T cells in vivo. Proc Natl Acad Sci USA. 1994;91(8):3077–3081.
   PubMed Web of Science ®Google Scholar
• van Bruggen I, Robertson TA, Papadimitriou JM. The effect of mild hyperthermia on the morphology and function of murine resident peritoneal macrophages. Exp Mol Pathol. 1991;55(2):119–134.
   PubMed Web of Science ®Google Scholar
• Vogl TJ, Wissniowski TT, Naguib NN, et al. Activation of tumor-specific T lymphocytes after laser-induced thermotherapy in patients with colorectal liver metastases. Cancer Immunol Immunother. 2009;58(10):1557–1563.
   PubMed Web of Science ®Google Scholar
• Wolfers J, Lozier A, Raposo G, et al. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med. 2001;7(3):297–303.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Zheng L. Tumor immunotherapy based on tumor-derived heat shock proteins. Oncol Lett. 2013;6(6):1543–1549.
   PubMed Web of Science ®Google Scholar
• Zheng H, Benjamin IJ, Basu S, et al. Heat shock factor 1-independent activation of dendritic cells by heat shock: implication for the uncoupling of heat-mediated immunoregulation from the heat shock response. Eur J Immunol. 2003;33(6):1754–1762.
   PubMed Web of Science ®Google Scholar
• Zhong H, Yang Y, Ma S, et al. Induction of a tumour-specific CTL response by exosomes isolated from heat-treated malignant ascites of gastric cancer patients. Int J Hyperthermia. 2011;27(6):604–611.
   PubMed Web of Science ®Google Scholar
• Ellis RJ. Protein misassembly: macromolecular crowding and molecular chaperones. Adv Exp Med Biol. 2007;594:1–13.
   PubMed Web of Science ®Google Scholar
• Asea A, Kraeft SK, Kurt-Jones EA, et al. HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med. 2000;6(4):435–442.
   PubMed Web of Science ®Google Scholar
• Multhoff G, Botzler C, Jennen L, et al. Heat shock protein 72 on tumor cells: a recognition structure for natural killer cells. J Immunol. 1997;158(9):4341–4350.
   PubMed Web of Science ®Google Scholar
• Wallin RP, Lundqvist A, More SH, et al. Heat-shock proteins as activators of the innate immune system. Trends Immunol. 2002;23(3):130–135.
   PubMed Web of Science ®Google Scholar
• Kunisawa J, Shastri N. Hsp90alpha chaperones large C-terminally extended proteolytic intermediates in the MHC class I antigen processing pathway. Immunity. 2006;24(5):523–534.
   PubMed Web of Science ®Google Scholar
• Javid B, MacAry PA, Lehner PJ. Structure and function: heat shock proteins and adaptive immunity. J Immunol. 2007;179(4):2035–2040.
   PubMed Web of Science ®Google Scholar
• Tamura Y, Peng P, Liu K, et al. Immunotherapy of tumors with autologous tumor-derived heat shock protein preparations. Science. 1997;278(5335):117–120.
   PubMed Web of Science ®Google Scholar
• Chen T, Guo J, Yang M, et al. Chemokine-containing exosomes are released from heat-stressed tumor cells via lipid raft-dependent pathway and act as efficient tumor vaccine. J Immunol. 2011;186(4):2219–2228.
   PubMed Web of Science ®Google Scholar
• Dai S, Wan T, Wang B, et al. More efficient induction of HLA-A*0201-restricted and carcinoembryonic antigen (CEA)-specific CTL response by immunization with exosomes prepared from heat-stressed CEA-positive tumor cells. Clin Cancer Res. 2005;11(20):7554–7563.
   PubMed Web of Science ®Google Scholar
• Isbert C, Ritz JP, Roggan A, et al. Enhancement of the immune response to residual intrahepatic tumor tissue by laser-induced thermotherapy (LITT) compared to hepatic resection. Lasers Surg Med. 2004;35(4):284–292.
   PubMed Web of Science ®Google Scholar
• Ivarsson K, Myllymaki L, Jansner K, et al. Resistance to tumour challenge after tumour laser thermotherapy is associated with a cellular immune response. Br J Cancer. 2005;93(4):435–440.
   PubMed Web of Science ®Google Scholar
• Yanase M, Shinkai M, Honda H, et al. Antitumor immunity induction by intracellular hyperthermia using magnetite cationic liposomes. Jpn J Cancer Res. 1998;89(7):775–782.
   PubMedGoogle Scholar
• Nah BS, Choi IB, Oh WY, et al. Vascular thermal adaptation in tumors and normal tissue in rats. Int J Radiat Oncol Biol Phys. 1996;35(1):95–101.
   PubMed Web of Science ®Google Scholar
• Meyer RE, Braun RD, Rosner GL, et al. Local 42 degrees C hyperthermia improves vascular conductance of the R3230Ac rat mammary adenocarcinoma during sodium nitroprusside infusion. Radiat Res. 2000;154(2):196–201.
   PubMed Web of Science ®Google Scholar
• Shakil A, Osborn JL, Song CW. Changes in oxygenation status and blood flow in a rat tumor model by mild temperature hyperthermia. Int J Radiat Oncol Biol Phys. 1999;43(4):859–865.
   PubMed Web of Science ®Google Scholar
• Shivers RR, Wijsman JA. Blood-brain barrier permeability during hyperthermia. Prog Brain Res. 1998;115:413–424.
   PubMed Web of Science ®Google Scholar
• Leuthardt EC, Duan C, Kim MJ, et al. Hyperthermic laser ablation of recurrent glioblastoma leads to temporary disruption of the peritumoral blood brain barrier. PLoS One. 2016;11(2):e0148613.
   PubMed Web of Science ®Google Scholar
• McDannold N, Vykhodtseva N, Jolesz FA, et al. MRI investigation of the threshold for thermally induced blood-brain barrier disruption and brain tissue damage in the rabbit brain. Magn Reson Med. 2004;51(5):913–923.
   PubMed Web of Science ®Google Scholar
• Kiyatkin EA, Sharma HS. Permeability of the blood-brain barrier depends on brain temperature. Neuroscience. 2009;161(3):926–939.
   PubMed Web of Science ®Google Scholar
• Lampson LA. Monoclonal antibodies in neuro-oncology: Getting past the blood-brain barrier. MAbs. 2011;3(2):153–160.
   PubMed Web of Science ®Google Scholar
• Husain B, Ellerman D. Expanding the boundaries of biotherapeutics with bispecific antibodies. BioDrugs. 2018;32(5):441–464.
   PubMed Web of Science ®Google Scholar
• Romani M, Pistillo MP, Carosio R, et al. Immune checkpoints and innovative therapies in glioblastoma. Front Oncol. 2018;8:464.
   PubMed Web of Science ®Google Scholar
• Galea I, Bernardes-Silva M, Forse PA, et al. An antigen-specific pathway for CD8 T cells across the blood-brain barrier. J Exp Med. 2007;204(9):2023–2030.
   PubMed Web of Science ®Google Scholar
• Miller RC, Roizin-Towle L, Komatsu K, et al. Interaction of heat with X-rays and cis-platinum; cell lethality and oncogenic transformation. Int J Hyperthermia. 1989;5(6):697–705.
   PubMed Web of Science ®Google Scholar
• Baker D, Sager H, Constable W. The influence of levamisole and hyperthermia on the incidence of metastases from an X-irradiated tumor. Cancer Invest. 1986;4(4):287–292.
   PubMed Web of Science ®Google Scholar
• Morita M, Kuwano H, Araki K, et al. Prognostic significance of lymphocyte infiltration following preoperative chemoradiotherapy and hyperthermia for esophageal cancer. Int J Radiat Oncol Biol Phys. 2001;49(5):1259–1266.
   PubMed Web of Science ®Google Scholar
• Moy AJ, Tunnell JW. Combinatorial immunotherapy and nanoparticle mediated hyperthermia. Adv Drug Deliv Rev. 2017;114:175–183.
   PubMed Web of Science ®Google Scholar
• Bear AS, Kennedy LC, Young JK, Perna SK, et al. Elimination of metastatic melanoma using gold nanoshell-enabled photothermal therapy and adoptive T cell transfer. PLoS One. 2013;8(7):e69073.
   PubMed Web of Science ®Google Scholar
• Wang C, Xu L, Liang C, et al. Immunological responses triggered by photothermal therapy with carbon nanotubes in combination with anti-CTLA-4 therapy to inhibit cancer metastasis. Adv Mater Weinheim. 2014;26(48):8154–8162.
   PubMed Web of Science ®Google Scholar
• Han X, Wang R, Xu J, et al. In situ thermal ablation of tumors in combination with nano-adjuvant and immune checkpoint blockade to inhibit cancer metastasis and recurrence. Biomaterials. 2019;224:119490.
   PubMed Web of Science ®Google Scholar
• Luo L, Zhu C, Yin H, et al. Laser immunotherapy in combination with perdurable PD-1 blocking for the treatment of metastatic tumors. ACS Nano. 2018;12(8):7647–7662.
   PubMed Web of Science ®Google Scholar
• Cano-Mejia J, Burga RA, Sweeney EE, et al. Prussian blue nanoparticle-based photothermal therapy combined with checkpoint inhibition for photothermal immunotherapy of neuroblastoma. Nanomed Nanotechnol Biol Med. 2017;13(2):771–781.
   PubMed Web of Science ®Google Scholar
• Chen Q, Xu L, Liang C, et al. Photothermal therapy with immune-adjuvant nanoparticles together with checkpoint blockade for effective cancer immunotherapy. Nat Commun. 2016;7:13193.
   PubMed Web of Science ®Google Scholar
• Liu Y, Chongsathidkiet P, Crawford BM, et al. Plasmonic gold nanostar-mediated photothermal immunotherapy for brain tumor ablation and immunologic memory. Immunotherapy. 2019;11(15):1293–1302.
   PubMed Web of Science ®Google Scholar
• Paiva MB, Sercarz JA, Pantuck AJ, et al. Combined cytoreductive laser therapy and immunotherapy for palliation of metastatic renal cell carcinoma to the head and neck. Lasers Med Sci. 2007;22(1):60–63.
   PubMed Web of Science ®Google Scholar
• Qiao G, Wang X, Zhou X, et al. Immune correlates of clinical benefit in a phase I study of hyperthermia with adoptive T cell immunotherapy in patients with solid tumors. Int J Hyperthermia. 2019;36(suppl 1):74–82.
   PubMed Web of Science ®Google Scholar
• Avelumab with laser interstitial therapy for recurrent glioblastoma. Available from: https://ClinicalTrials.gov/show/NCT03341806.
   Google Scholar
• LITT and pembrolizumab in recurrent brain metastasis. Available from: https://ClinicalTrials.gov/show/NCT04187872.
   Google Scholar
• Laser interstitial thermotherapy (LITT) combined with checkpoint inhibitor for recurrent GBM (RGBM). Available from: https://ClinicalTrials.gov/show/NCT03277638.
   Google Scholar