Could hyperthermia with proton therapy mimic carbon ion therapy? Exploring a thermo-radiobiological rationale

References

• Overgaard J. The heat is (still) on – The past and future of hyperthermic radiation oncology. Radiother Oncol 2013;109:185–7
   PubMed Web of Science ®Google Scholar
• Wust P, Hildebrandt B, Sreenivasa G, Rau B, Gellermann J, Ries H, et al. Hyperthermia in combined treatment of cancer. Lancet Oncol 2002;3:487–97
   PubMed Web of Science ®Google Scholar
• Horsman MR, Overgaard J. Hyperthermia: A potent enhancer of radiotherapy. Clin Oncol 2007;19:418–26
   PubMed Web of Science ®Google Scholar
• Dewhirst MW, Prosnitz L, Thrall D, Prescott D, Clegg S, Charles C, et al. Hyperthermic treatment of malignant diseases: Current status and a view toward the future. Semin Oncol 1997;24:616–25
   PubMed Web of Science ®Google Scholar
• Dewhirst MW, Vujaskovic Z, Jones E, Thrall D. Re-setting the biologic rationale for thermal therapy. Int J Hyperthermia 2005;21:779–90
   PubMed Web of Science ®Google Scholar
• Roti Roti JL. Cellular responses to hyperthermia (40–46 °C): Cell killing and molecular events. Int J Hyperthermia 2008;24:3–15
   PubMed Web of Science ®Google Scholar
• Schildkopf P, Ott OJ, Frey B, Wadepohl M, Sauer R, Fietkau R, et al. Biological rationales and clinical applications of temperature controlled hyperthermia – Implications for multimodal cancer treatments. Curr Med Chem 2010;17:3045–57
   PubMed Web of Science ®Google Scholar
• Zölzer F, Streffer C. Radiation and/or hyperthermia sensitivity of human melanoma cells grown for several days in media with reduced pH. Strahlenther Onkol 1999;175:325–32
   PubMedGoogle Scholar
• Raaphorst GP, Ng CE, Yang DP. Thermal radiosensitization and repair inhibition in human melanoma cells: A comparison of survival and DNA double strand breaks. Int J Hyperthermia 1999;15:17–27
   PubMed Web of Science ®Google Scholar
• Raaphorst GP, Mao JP, Ng CE. Sublethal radiation damage repair and its inhibition by hyperthermia in two human melanoma cell lines of different radiosensitivities. Melanoma Res 1994;4:157–61
   PubMed Web of Science ®Google Scholar
• Raaphorst GP, Bussey A, Heller DP, Ng CE. Comparison of thermoradiosensitization in two human melanoma cell lines and one fibroblast cell line by concurrent mild hyperthermia and low-dose-rate irradiation. Radiat Res 1994;137:338–45
   PubMed Web of Science ®Google Scholar
• Huang T, Gong W, Li X, Zou C, Jiang G, Li X, et al. Enhancement of osteosarcoma cell sensitivity to cisplatin using paclitaxel in the presence of hyperthermia. Int J Hyperthermia 2013;29:248–55
   PubMed Web of Science ®Google Scholar
• Kubista B, Trieb K, Blahovec H, Kotz R, Micksche M. Hyperthermia increases the susceptibility of chondro- and osteosarcoma cells to natural killer cell-mediated lysis. Anticancer Res 2002;22:789–92
   PubMed Web of Science ®Google Scholar
• Thiesen B, Jordan A. Clinical applications of magnetic nanoparticles for hyperthermia. Int J Hyperthermia 2008;24:467–74
   PubMed Web of Science ®Google Scholar
• Frey B, Weiss EM, Rubner Y, Wunderlich R, Ott OJ, Sauer R, et al. Old and new facts about hyperthermia-induced modulations of the immune system. Int J Hyperthermia 2012;28:528–42
   PubMed Web of Science ®Google Scholar
• Chatterjee DK, Diagaradjane P, Krishnan S. Nanoparticle-mediated hyperthermia in cancer therapy. Ther Deliv 2011;2:1001–14
   PubMedGoogle Scholar
• Krishnan S, Diagaradjane P, Cho SH. Nanoparticle-mediated thermal therapy: Evolving strategies for prostate cancer therapy. Int J Hyperthermia 2010;26:775–89
   PubMed Web of Science ®Google Scholar
• Fani F, Schena E, Saccomandi P, Silvestri S. CT-based thermometry: An overview. Int J Hyperthermia 2014;30:219–27
   PubMed Web of Science ®Google Scholar
• Numan WC, Hofstetter LW, Kotek G, Bakker JF, Fiveland EW, Houstan GC, et al. Exploration of MR-guided head and neck hyperthermia by phantom testing of a modified prototype applicator for use with proton resonance frequency shift thermometry. Int J Hyperthermia 2014;30:184–91
   PubMed Web of Science ®Google Scholar
• Verhaart RF, Fortunati V, Verduijn GM, van Walsum T, Veenland JF, Paulides MM. CT-based patient modelling for head and neck hyperthermia treatment planning: manual versus automatic normal-tissue segmentation. Radiother Oncol 2014;111:158–63
   PubMed Web of Science ®Google Scholar
• Kok HP, Crezee J, Franken NA, Stalpers LJ, Barendsen GW, Bel A. Quantifying the combined effect of radiation therapy and hyperthermia in terms of equivalent dose distributions. Int J Radiat Oncol Biol Phys 2014;88:739–45
   PubMed Web of Science ®Google Scholar
• Rijnen Z, Bakker JF, Canters RA, Togni P, Verduijn GM, Levendag PC, et al. Clinical integration of software tool VEDO for adaptive and quantitative application of phased array hyperthermia in the head and neck. Int J Hyperthermia 2013;29:181–93
   PubMed Web of Science ®Google Scholar
• Issels RD, Lindner LH, Verweij J, Wust P, Reichardt P, Schem BC, et al. Neo-adjuvant chemotherapy alone or with regional hyperthermia for localized high-risk soft-tissue sarcoma: A randomized phase 3 multicentre study. Lancet Oncol 2010;11:561–70
   PubMed Web of Science ®Google Scholar
• Wesslowski R, Schneider DT, Mils O, Friemann V, Kyrillopoulou O, Schaper J, et al. Regional deep hyperthermia for salvage treatment of children and adolescents with refractory or recurrent non-testicular malignant germ-cell tumours: An open-label, non-randomised, single-institution, phase 2 study. Lancet Oncol 2013;14:843–52
   PubMedGoogle Scholar
• Wittlinger M, Rödel CM, Weiss C, Krause SF, Kühn R, Fietkau R, et al. Quadrimodal treatment of high-risk T1 and T2 bladder cancer: Transurethral tumour resection followed by concurrent radiochemotherapy and regional deep hyperthermia. Radiother Oncol 2009;93:358–63
   PubMed Web of Science ®Google Scholar
• Jermann M. Particle therapy statistics in 2013. Int J Particle Ther 2014;1:40–3
   Google Scholar
• Kerstiens J, Johnstone PA. Proton therapy expansion under current United States reimbursement models. Int J Radiat Oncol Biol Phys 2014;89:235–40
   PubMedGoogle Scholar
• Nyström H, Blomqvist E, Hǿyer M, Montelius A, Muren LP, Nilsson P, et al. Particle therapy – A next logical step in the improvement of radiotherapy. Acta Oncol 2011;50:741–4
   PubMed Web of Science ®Google Scholar
• Wilkens JJ, Oelfke U. Direct comparison of biologically optimized spread-out Bragg peaks for protons and carbon ions. Int J Radiat Oncol Biol Phys 2008;70:262–6
   PubMed Web of Science ®Google Scholar
• Suit H, DeLaney T, Goldberg S, Paganetti H, Clasie B, Gerweck L, et al. Proton vs carbon beam ions in the definitive radiation treatment of cancer patients. Radiother Oncol 2010;95:3–22
   PubMed Web of Science ®Google Scholar
• Paganetti H, Niemierko A, Ancukiewicz M, Gerweck LE, Goitein M, Loeffler JS, et al. Relative biological effectiveness (RBE) values for proton beam therapy. Int J Radiat Oncol Biol Phys 2002;53:407–21
   PubMed Web of Science ®Google Scholar
• Carabe A. Radiobiology of proton and carbon ion therapy. In: Charlie Ma C-M, Lomax T, eds. Proton and carbon ion therapy. BocaRaton, FL: Taylor & Francis Group, CRC Press, 2013, pp. 71–98
   Google Scholar
• Frese MC, Yu VK, Stewart RD, Carlson DJ. A mechanism-based approach to predict the relative biological effectiveness of protons and carbon ions in radiation therapy. Int J Radiat Oncol Biol Phys 2012;83:442–50
   PubMed Web of Science ®Google Scholar
• Allen C, Borak TB, Tsujii H, Nickoloff JA. Heavy charged particle radiobiology: Using enhanced biological effectiveness and improved beam focusing to advance cancer therapy. Mutat Res 2011;711:150–7
   PubMed Web of Science ®Google Scholar
• Schlaff CD, Krauze A, Belard A, O’Connell JJ, Camphausen KA. Bringing the heavy: Carbon ion therapy in the radiobiological and clinical context. Radiat Oncol 2014;9:88 . doi:10.1186/1748-717X-9-88
   PubMed Web of Science ®Google Scholar
• Furusawa Y, Fukutsu K, Aoki M, Itsukaichi H, Eguchi-Kasai K, Ohara H, et al. Inactivation of aerobic and hypoxic cells from three different cell lines by accelerated (3)He, (12)C and (20)Ne-ion beams. Radiat Res 2000;154:485–96
   PubMed Web of Science ®Google Scholar
• Blakely E. Biology of Bevlac beam: Cellular studies. In: Skarsgard L, ed. Pion and heavy ion radiation therapy: Pre-clinical and clinical studies. Amsterdam: Elsevier, 1982, pp. 229–50
   Google Scholar
• Baumann M, Krause M, Hill R. Exploring the role of cancer stem cells in radioresistance. Nat Rev Cancer 2008;8:545–54
   PubMed Web of Science ®Google Scholar
• Rycaj K, Tang DG. Cancer stem cells and radioresistance. Int J Radiat Biol 2014;90:615–21
   PubMed Web of Science ®Google Scholar
• Cui X, Oonishi K, Tsujii H, Yasuda T, Matsumoto Y, Furusawa Y, et al. Effects of carbon ion beam on putative colon cancer stem cells and its comparison with X-rays. Cancer Res 2011;71:3676–87
   PubMed Web of Science ®Google Scholar
• Ogawa K, Yoshioka Y, Isohashi F, Seo Y, Yoshida K, Yamazaki H. Radiotherapy targeting cancer stem cells: Current views and future perspectives. Anticancer Res 2013;33:747–54
   PubMed Web of Science ®Google Scholar
• Hamada N. Recent insights into the biological action of heavy-ion radiation. J Radiat Res 2009;50:1–9
   PubMed Web of Science ®Google Scholar
• Masunaga S, Ando K, Uzawa A, Hirayama R, Furusawa Y, Koike S, et al. The radiosensitivity of total and quiescent cell populations in solid tumors to 290 MeV/µ carbon ion beam irradiation in vivo. Acta Oncol 2008;47:1087–93
   PubMed Web of Science ®Google Scholar
• Takahashi M, Hirakawa H, Yajima H, Izumi-Nakajima N, Okayasu R, Fujimori A. Carbon beam is more effective to induce cell death in sphere-type A172 human glioblastoma cells compared with X-rays. Int J Radiat Biol 2014;11:1–8 [Epub ahead of print]
   Google Scholar
• Peschke P, Karger CP, Scholz M, Debus J, Huber PE. Relative biological effectiveness of carbon ions for local tumor control of a radioresistant prostate carcinoma in the rat. Int J Radiat Oncol Biol Phys 2011;79:239–46
   PubMed Web of Science ®Google Scholar
• Takahashi A, Kubo M, Ma H, Nakagawa A, Yoshida Y, Isono M, et al. NHEJ repair plays a more important role than homologous recombination repair in defining radiosensitivity after exposure to high-LET radiation. Radiat Res 2014;182:338–44
   Google Scholar
• Robinson JE, Wizenberg MJ, McCready WA. Combined hyperthermia and radiation suggest an alternative to heavy particle therapy for reduced oxygen enhancement ratios. Nature 1974;251:521–2
   PubMed Web of Science ®Google Scholar
• Corry PM, Armour EP. The heat shock response: Role in radiation biology and cancer therapy. Int J Hyperthermia 2005;21:769–78
   PubMed Web of Science ®Google Scholar
• Gerner EW, Leith JT. Interaction of hyperthermia with radiations of different linear energy transfer. Int J Radiat Biol 1977;31:283–8
   Google Scholar
• Chang PY, Tobias CA, Blakely EA. Protein synthesis modulates the biological effectiveness of the combined action of hyperthermia and high-LET radiation. Radiat Res 1992;129:272–80
   PubMedGoogle Scholar
• Ohnishi T, Takahashi A, Yano T, Matsumoto H, Wang X, Ohnishi K, et al. Hyperthermic enhancement of tumour growth inhibition by accelerated carbon-ions in transplantable human esophageal cancer. Int J Hyperthermia 1998;14:195–202
   PubMed Web of Science ®Google Scholar
• Riedel KG, Svitra PP, Seddon JM, Albert DM, Gragoudas ES, Koehler AM, et al. Proton beam irradiation and hyperthermia. Effects on experimental choroidal melanoma. Arch Opthalmol 1985;103:1862–69
   PubMedGoogle Scholar
• Hyperthermia and protons in unresectable soft tissue sarcoma (HYPROSAR) 2014. Available at http://clinicaltrials.gov/show/NCT01904565 (accessed 28 June 2014)
   Google Scholar
• Prosnitz LR, Maguire P, Anderson JM, Scully SP, Harrelson JM, Jones EL, et al. The treatment of high-grade soft tissue sarcomas with preoperative thermoradiotherapy. Int J Radiat Oncol Biol Phys 1999;45:941–9
   PubMed Web of Science ®Google Scholar
• Puric E, Bodis S. Stellenwert der Hyperthermia in der Sarkomtherapie. Schweiz Z Onkol 2012;2:18–22
   Google Scholar
• Weber DC, Rutz HP, Bolsi A, Pedroni E, Coray A, Jermann M, et al. Spot scanning proton therapy in the curative treatment of adult patients in sarcoma: The Paul Scherrer Institute experience. Int J Radiat Oncol Biol Phys 2007;69:865–71
   PubMed Web of Science ®Google Scholar
• Kamada T, Tsujii H, Tsuji H, Yanagi T, Mizoe JE, Miyamoto T, et al. Efficacy and safety of carbon ion radiotherapy in bone and soft tissue sarcomas. J Clin Oncol 2002;20:4466–71
   PubMed Web of Science ®Google Scholar
• Tsujii H, Kamada T. A review of update clinical results of carbon ion radiotherapy. Jpn J Clin Oncol 2012;42:670–85
   PubMed Web of Science ®Google Scholar
• Sugahara S, Kamada T, Imai R, Tsuji H, Kameda N, Okada T, et al. Carbon ion radiotherapy for localized primary sarcoma of the extremities: Results of a phase I/II trial. Radiother Oncol 2012;105:226–31
   PubMed Web of Science ®Google Scholar
• Joiner M, van der Kogel A. eds. Basic Clinical Radiobiology. London: Hodder Arnold, 2009
   Google Scholar
• IAEA. Radiation biology: A handbook for teachers and students. Training Course Series 42. Vienna: IAEA, 2010. Available at http://www-pub.iaea.org/MTCD/publications/PDF/TCS-42_web.pdf (accessed 3 September 2014)
   Google Scholar