Mild temperature hyperthermia and radiation therapy: Role of tumour vascular thermotolerance and relevant physiological factors

References

• Song CW, Park HJ, Lee CK, Griffin R. Implications of increased tumor blood flow and oxygenation caused by mild temperature hyperthermia in tumor treatment. Int J Hyperthermia 2005; 21: 761–767
   PubMed Web of Science ®Google Scholar
• Song CW. Effect of local hyperthermia on blood flow and microenvironment: A review. Cancer Res 1984; 44: S4721–S4730
   PubMed Web of Science ®Google Scholar
• Dewey WC, Thrall DE, Gillette EL. Hyperthermia and radiation–a selective thermal effect on chronically hypoxic tumor cells in vivo. Int J Radiat Oncol Biol Phys 1977; 2: 99–103
   PubMed Web of Science ®Google Scholar
• Westermann AM, Jones EL, Schem BC, van der Steen-Banasik EM, Koper P, Mella O, Uitterhoeve AL, de Wit R, van der Velden J, Burger C, et al. First results of triple-modality treatment combining radiotherapy, chemotherapy, and hyperthermia for the treatment of patients with stage IIB, III, and IVA cervical carcinoma. Cancer 2005; 104(4)763–770
   PubMed Web of Science ®Google Scholar
• Song CW, Rhee JG, Haumschild DJ. Continuous and non-invasive quantification of heat-induced changes in blood flow in the skin and RIF-1 tumour of mice by laser Doppler flowmetry. Int J Hyperthermia 1987; 3: 71–77
   PubMed Web of Science ®Google Scholar
• Vujaskovic Z, Poulson JM, Gaskin AA, Thrall DE, Page RL, Charles HC, MacFall JR, Brizel DM, Meyer RE, Prescott DM, et al. Temperature-dependent changes in physiologic parameters of spontaneous canine soft tissue sarcomas after combined radiotherapy and hyperthermia treatment. Int J Radiat Oncol Biol Phys 2000; 46(1)179–185
   PubMed Web of Science ®Google Scholar
• Thrall DE, Larue SM, Pruitt AF, Case B, Dewhirst MW. Changes in tumour oxygenation during fractionated hyperthermia and radiation therapy in spontaneous canine sarcomas. Int J Hyperthermia 2006; 22: 365–373
   PubMed Web of Science ®Google Scholar
• Song CW, Shakil A, Griffin RJ, Okajima K. Improvement of tumor oxygenation status by mild temperature hyperthermia alone or in combination with carbogen. Semin Oncol 1997; 24: 626–632
   PubMed Web of Science ®Google Scholar
• Acker JC, Dewhirst MW, Honore GM, Samulski TV, Tucker JA, Oleson JR. Blood perfusion measurements in human tumours: Evaluation of laser Doppler methods. Int J Hyperthermia 1990; 6: 287–304
   PubMed Web of Science ®Google Scholar
• Griffin RJ, Okajima K, Song CW. The optimal combination of hyperthermia and carbogen breathing to increase tumor oxygenation and radiation response. Int J Radiat Oncol Biol Phys 1998; 42: 865–869
   PubMed Web of Science ®Google Scholar
• Iwata K, Shakil A, Hur WJ, Makepeace CM, Griffin RJ, Song CW. Tumour pO2 can be increased markedly by mild hyperthermia. Br J Cancer Suppl 1996; 27: S217–S221
   PubMedGoogle 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: 859–865
   PubMed Web of Science ®Google Scholar
• Song CW, Park H, Griffin RJ. Improvement of tumor oxygenation by mild hyperthermia. Radiat Res 2001; 155: 515–528
   PubMed Web of Science ®Google Scholar
• Thews O, Li Y, Kelleher DK, Chance B, Vaupel P. Microcirculatory function, tissue oxygenation, microregional redox status and ATP distribution in tumors upon localized infrared-A-hyperthermia at 42°C. Adv Exp Med Biol 2003; 530: 237–247
   PubMed Web of Science ®Google Scholar
• Vaupel P, Okunieff P, Kluge M. Response of tumour red blood cell flux to hyperthermia and/or hyperglycaemia. Int J Hyperthermia 1989; 5: 199–210
   PubMed Web of Science ®Google Scholar
• Vaupel P, Kallinowski F. Physiological effects of hyperthermia. Recent Results Cancer Res 1987; 104: 71–109
   PubMedGoogle Scholar
• Oleson JR. Eugene Robertson Special Lecture. Hyperthermia from the clinic to the laboratory: A hypothesis. Int J Hyperthermia 1995; 11: 315–322
   PubMed Web of Science ®Google Scholar
• Song CW, Lin JC, Chelstrom LM, Levitt SH. The kinetics of vascular thermotolerance in SCK tumors of A/J mice. Int J Radiat Oncol Biol Phys 1989; 17: 799–802
   PubMed Web of Science ®Google Scholar
• Lin JC, Song CW. Influence of vascular thermotolerance on the heat-induced changes in blood flow, pO2, and cell survival in tumors. Cancer Res 1993; 53: 2076–2080
   PubMed Web of Science ®Google Scholar
• Nah BS, Choi IB, Oh WY, Osborn JL, Song CW. Vascular thermal adaptation in tumors and normal tissue in rats. Int J Radiat Oncol Biol Phys 1996; 35: 95–101
   PubMed Web of Science ®Google Scholar
• Dewhirst MW, Kimura H, Rehmus SW, Braun RD, Papahadjopoulos D, Hong K, Secomb TW. Microvascular studies on the origins of perfusion-limited hypoxia. Br J Cancer Suppl 1996; 27: S247–S251
   PubMedGoogle Scholar
• Chaplin DJ, Trotter MJ, Durand RE, Olive PL, Minchinton AI. Evidence for intermittent radiobiological hypoxia in experimental tumour systems. Biomed Biochim Acta 1989; 48: S255–S259
   PubMedGoogle Scholar
• Horsman MR, Nordsmark M, Khalil AA, Hill SA, Chaplin DJ, Siemann DW, Overgaard J. Reducing acute and chronic hypoxia in tumours by combining nicotinamide with carbogen breathing. Acta Oncol 1994; 33: 371–376
   PubMed Web of Science ®Google Scholar
• Hill SA, Pigott KH, Saunders MI, Powell ME, Arnold S, Obeid A, Ward G, Leahy M, Hoskin PJ, Chaplin DJ. Microregional blood flow in murine and human tumours assessed using laser Doppler microprobes. Br J Cancer Suppl 1996; 27: S260–S263
   PubMedGoogle Scholar
• Janssen HL, Haustermans KM, Sprong D, Blommestijn G, Hofland I, Hoebers FJ, Blijweert E, Raleigh JA, Semenza GL, Varia MA, et al. HIF-1A, pimonidazole, and iododeoxyuridine to estimate hypoxia and perfusion in human head-and-neck tumors. Int J Radiat Oncol Biol Phys 2002; 54(5)1537–1549
   PubMed Web of Science ®Google Scholar
• Trotter MJ, Chaplin DJ, Olive PL. Effect of angiotensin II on intermittent tumour blood flow and acute hypoxia in the murine SCCVII carcinoma. Eur J Cancer 1991; 27: 887–893
   PubMed Web of Science ®Google Scholar
• Chaplin DJ, Olive PL, Durand RE. Intermittent blood flow in a murine tumor: Radiobiological effects. Cancer Res 1987; 47: 597–601
   PubMed Web of Science ®Google Scholar
• Bicher HI, Hetzel FW, Sandhu TS, Frinak S, Vaupel P, O'Hara MD, O'Brien T. Effects of hyperthermia on normal and tumor microenvironment. Radiology 1980; 137: 523–530
   PubMed Web of Science ®Google Scholar
• Vaupel PW, Otte J, Manz R. Oxygenation of malignant tumors after localized microwave hyperthermia. Radiat Environ Biophys 1982; 20: 289–300
   PubMed Web of Science ®Google Scholar
• Griffin RJ, Okajima K, Ogawa A, Song CW. Radiosensitization of two murine tumours with mild temperature hyperthermia and carbogen breathing. Int J Radiat Biol 1999; 75: 1299–1306
   PubMed Web of Science ®Google Scholar
• Griffin RJ, Ogawa A, Williams BW, Song CW. Hyperthermic enhancement of tumor radiosensitization strategies. Immunol Invest 2005; 34: 343–359
   PubMed Web of Science ®Google Scholar
• Kirkpatrick JP, Brizel DM, Dewhirst MW. A mathematical model of tumor oxygen and glucose mass transport and metabolism with complex reaction kinetics. Radiat Res 2003; 159: 336–344
   PubMed Web of Science ®Google Scholar
• Vaupel P, Ostheimer K, Muller-Klieser W. Circulatory and metabolic responses of malignant tumors during localized hyperthermia. J Cancer Res Clin Oncol 1980; 98: 15–29
   PubMed Web of Science ®Google Scholar
• Vujaskovic Z, Song CW. Physiological mechanisms underlying heat-induced radiosensitization. Int J Hyperthermia 2004; 20: 163–174
   PubMed Web of Science ®Google Scholar
• Okajima K, Griffin RJ, Iwata K, Shakil A, Song CW. Tumor oxygenation after mild-temperature hyperthermia in combination with carbogen breathing: Dependence on heat dose and tumor type. Radiat Res 1998; 149: 294–299
   PubMed Web of Science ®Google Scholar
• Rhee JG, Song CW, Levitt SH. Changes in thermosensitivity of mouse mammary carcinoma following hyperthermia in vivo. Cancer Res 1982; 42: 4485–4489
   PubMed Web of Science ®Google Scholar
• Song CW, Patten MS, Chelstrom LM, Rhee JG, Levitt SH. Effect of multiple heatings on the blood flow in RIF-1 tumours, skin and muscle of C3H mice. Int J Hyperthermia 1987; 3: 535–545
   PubMed Web of Science ®Google Scholar
• Campbell SD, Kruuv J, Lepock JR. Characterization and radiation response of a heat-resistant variant of V79 cells. Radiat Res 1983; 93: 51–61
   PubMed Web of Science ®Google Scholar
• Dikomey E, Jung H. Effect of thermotolerance and step-down heating on thermal radiosensitization in CHO cells. Int J Radiat Biol 1992; 61: 235–242
   PubMed Web of Science ®Google Scholar
• Fortin A, Raybaud-Diogene H, Tetu B, Deschenes R, Huot J, Landry J. Overexpression of the 27 KDa heat shock protein is associated with thermoresistance and chemoresistance but not with radioresistance. Int J Radiat Oncol Biol Phys 2000; 46: 1259–1266
   PubMed Web of Science ®Google Scholar
• Hartson-Eaton M, Malcolm AW, Hahn GM. Radiosensitivity and thermosensitization of thermotolerant Chinese hamster cells and RIF-1 tumors. Radiat Res 1984; 99: 175–184
   PubMed Web of Science ®Google Scholar
• Mackey MA, Anolik SL, Roti Roti JL. Changes in heat and radiation sensitivity during long duration, moderate hyperthermia in HeLa S3 cells. Int J Radiat Oncol Biol Phys 1992; 24: 543–550
   PubMed Web of Science ®Google Scholar
• Mivechi NF, Li GC. Lack of effect of thermotolerance on radiation response and thermal radiosensitization of murine bone marrow progenitors. Cancer Res 1987; 47: 1538–1541
   PubMed Web of Science ®Google Scholar
• Chaplin DJ, Horsman MR, Aoki DS. Nicotinamide, Fluosol DA and Carbogen: A strategy to reoxygenate acutely and chronically hypoxic cells in vivo. Br J Cancer 1991; 63: 109–113
   PubMed Web of Science ®Google Scholar
• Laurence VM, Ward R, Dennis IF, Bleehen NM. Carbogen breathing with nicotinamide improves the oxygen status of tumours in patients. Br J Cancer 1995; 72: 198–205
   PubMed Web of Science ®Google Scholar
• Rojas A, Joiner MC, Denekamp J. Extrapolations from laboratory and preclinical studies for the use of carbogen and nicotinamide in radiotherapy. Radiother Oncol 1992; 24: 123–124
   PubMed Web of Science ®Google Scholar
• Brizel DM, Lin S, Johnson JL, Brooks J, Dewhirst MW, Piantadosi CA. The mechanisms by which hyperbaric oxygen and carbogen improve tumour oxygenation. Br J Cancer 1995; 72: 1120–1124
   PubMed Web of Science ®Google Scholar
• Noth U, Rodrigues LM, Robinson SP, Jork A, Zimmermann U, Newell B, Griffiths JR. In vivo determination of tumor oxygenation during growth and in response to carbogen breathing using 15C5-loaded alginate capsules as fluorine-19 magnetic resonance imaging oxygen sensors. Int J Radiat Oncol Biol Phys 2004; 60(3)909–919
   PubMed Web of Science ®Google Scholar
• Robinson SP, Howe FA, Stubbs M, Griffiths JR. Effects of nicotinamide and carbogen on tumour oxygenation, blood flow, energetics and blood glucose levels. Br J Cancer 2000; 82: 2007–2014
   PubMed Web of Science ®Google Scholar
• Griffin RJ, Okajima K, Barrios B, Song CW. Mild temperature hyperthermia combined with carbogen breathing increases tumor partial pressure of oxygen (pO2) and radiosensitivity. Cancer Res 1996; 56: 5590–5593
   PubMed Web of Science ®Google Scholar
• Ogawa A, Griffin RJ, Song CW. Effect of a combination of mild-temperature hyperthermia and nicotinamide on the radiation response of experimental tumors. Radiat Res 2000; 153: 327–331
   PubMed Web of Science ®Google Scholar
• Dewhirst MW, Prosnitz L, Thrall D, Prescott D, Clegg S, Charles C, MacFall J, Rosner G, Samulski T, Gillette E, et al. Hyperthermic treatment of malignant diseases: Current status and a view toward the future. Semin Oncol 1997; 24(6)616–625
   PubMed Web of Science ®Google Scholar
• Kong G, Braun RD, Dewhirst MW. Characterization of the effect of hyperthermia on nanoparticle extravasation from tumor vasculature. Cancer Res 2001; 61: 3027–3032
   PubMed Web of Science ®Google Scholar
• Griffin RJ, Lee SH, Rood KL, Stewart MJ, Lyons JC, Lew YS, Park H, Song CW. Use of arsenic trioxide as an antivascular and thermosensitizing agent in solid tumors. Neoplasia 2000; 2(6)555–560
   PubMed Web of Science ®Google Scholar
• Kallinowski F, Zander R, Hoeckel M, Vaupel P. Tumor tissue oxygenation as evaluated by computerized-pO2-histography. Int J Radiat Oncol Biol Phys 1990; 19: 953–961
   PubMed Web of Science ®Google Scholar
• Vaupel P, Schlenger K, Knoop C, Hockel M. Oxygenation of human tumors: Evaluation of tissue oxygen distribution in breast cancers by computerized O2 tension measurements. Cancer Res 1991; 51: 3316–3322
   PubMed Web of Science ®Google Scholar
• Dings RP, Loren M, Heun H, McNiel E, Griffioen AW, Mayo KH, Griffin RJ. Scheduling of radiation with angiogenesis inhibitors anginex and Avastin improves therapeutic outcome via vessel normalization. Clin Cancer Res 2007; 13(11)3395–3402
   PubMed Web of Science ®Google Scholar
• Dings RP, Williams BW, Song CW, Griffioen AW, Mayo KH, Griffin RJ. Anginex synergizes with radiation therapy to inhibit tumor growth by radiosensitizing endothelial cells. Int J Cancer 2005; 115: 312–319
   PubMed Web of Science ®Google Scholar
• Dings RP, Yokoyama Y, Ramakrishnan S, Griffioen AW, Mayo KH. The designed angiostatic peptide anginex synergistically improves chemotherapy and antiangiogenesis therapy with angiostatin. Cancer Res 2003; 63: 382–385
   PubMed Web of Science ®Google Scholar