Hyperthermia with photon radiotherapy is thermoradiobiologically analogous to neutrons for tumors without enhanced normal tissue toxicity

References

• Goodhead DT. Neutrons are forever! Historical perspectives. Int J Radiat Biol. 2019;95:957–984.
   PubMed Web of Science ®Google Scholar
• Laramore GE. Neutron therapy and boron neutron capture therapy In: Halperin EC, Wazer DE, Perez CA, Brady LW, editors. Perez & Brady’s principles and practice of radiation oncology. Philadelphia (PA): Wolters Kluwer Health; 2018. p. 482–491.
   Google Scholar
• Wambersie A, Hendry J, Gueulette J, et al. Radiobiological rationale and patient selection for high-LET radiation in cancer therapy. Radiother Oncol. 2004;73(2):S1–S14.
   PubMed Web of Science ®Google Scholar
• Wambersie A, Richard F, Breteau N. Development of fast neutron therapy worldwide. Radiobiological, clinical and technical aspects. Acta Oncol. 1994;33(3):261–274.
   PubMed Web of Science ®Google Scholar
• Denekamp J. Neutron radiobiology revisited. Acta Oncol. 1994;33(3):233–240.
   PubMed Web of Science ®Google Scholar
• Vynckier S, Schmidt R. The physical basis for radiotherapy with neutrons. Recent Results Cancer Res. 1998;150:1–30.
   PubMedGoogle Scholar
• Laramore GE, Krall JM, Griffin TW, et al. Neutron versus photon irradiation for unresectable salivary gland tumors: final report of an RTOG-MRC randomized clinical trial. Radiation Therapy Oncology Group. Medical Research Council. Int J Radiat Oncol Biol Phys. 1993;27(2):235–240.
   PubMed Web of Science ®Google Scholar
• van der Zee J, Vujaskovic Z, Kondo M, et al. The Kadota Fund International Forum 2004–clinical group consensus. Int J Hyperthermia. 2008;24(2):111–122.
   PubMed Web of Science ®Google Scholar
• Dewhirst MW, Lee CT, Ashcraft KA. The future of biology in driving the field of hyperthermia. Int J Hyperthermia. 2016;32(1):4–13.
   PubMed Web of Science ®Google Scholar
• Datta NR, Ordonez SG, Gaipl US, et al. Local hyperthermia combined with radiotherapy and-/or chemotherapy: recent advances and promises for the future. Cancer Treat Rev. 2015;41(9):742–753.
   PubMed Web of Science ®Google Scholar
• Overgaard J. The heat is (still) on–the past and future of hyperthermic radiation oncology. Radiother Oncol. 2013;109(2):185–187.
   PubMed Web of Science ®Google Scholar
• Peeken JC, Vaupel P, Combs SE. Integrating hyperthermia into modern radiation oncology: what evidence is necessary? Front Oncol. 2017;7:132.
   PubMed Web of Science ®Google Scholar
• Datta NR, Puric E, Schneider R, et al. Could hyperthermia with proton therapy mimic carbon ion therapy? Exploring a thermo-radiobiological rationale. Int J Hyperthermia. 2014;30(7):524–530.
   PubMed Web of Science ®Google Scholar
• Robinson JE, Wizenberg MJ, McCready WA. Combined hyperthermia and radiation suggest and alternative to heavy particle therapy for reduced oxygen enhancement ratios. Nature. 1974;251(5475):521–522.
   PubMed Web of Science ®Google Scholar
• Horsman MR, Overgaard J. Hyperthermia: a potent enhancer of radiotherapy. Clin Oncol (R Coll Radiol). 2007;19(6):418–426.
   PubMed Web of Science ®Google Scholar
• Repasky EA, Evans SS, Dewhirst MW. Temperature matters! And why it should matter to tumor immunologists. Cancer Immunol Res. 2013;1(4):210–216.
   PubMed Web of Science ®Google Scholar
• Frey B, Weiss EM, 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
• 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
• Datta NR, Puric E, Klingbiel D, et al. Hyperthermia and radiation therapy in locoregional recurrent breast cancers: a systematic review and meta-analysis. Int J Radiat Oncol Biol Phys. 2016;94(5):1073–1087.
   PubMed Web of Science ®Google Scholar
• Datta NR, Rogers S, Klingbiel D, et al. Hyperthermia and radiotherapy with or without chemotherapy in locally advanced cervical cancer: a systematic review with conventional and network meta-analyses. Int J Hyperthermia. 2016;32(7):809–821.
   PubMed Web of Science ®Google Scholar
• Datta NR, Rogers S, Ordonez SG, et al. Hyperthermia and radiotherapy in the management of head and neck cancers: a systematic review and meta-analysis. Int J Hyperthermia. 2016;32(1):31–40.
   PubMed Web of Science ®Google Scholar
• Datta NR, Bodis S. Hyperthermia with radiotherapy reduces tumour alpha/beta: insights from trials of thermoradiotherapy vs radiotherapy alone. Radiother Oncol. 2019;138:1–8.
   PubMed Web of Science ®Google Scholar
• Issels RD, Lindner LH, Verweij J, et al. Effect of Neoadjuvant chemotherapy plus regional hyperthermia on long-term outcomes among patients with localized high-risk soft tissue sarcoma: the EORTC 62961-ESHO 95 randomized clinical trial. JAMA Oncol. 2018;4(4):483–492.
   PubMed Web of Science ®Google Scholar
• Emami B, Song CW. Physiological mechanisms in hyperthermia: a review. Int J Radiat Oncol Biol Phys. 1984;10(2):289–295.
   PubMed Web of Science ®Google Scholar
• Vaupel PW, Kelleher DK. Pathophysiological and vascular characteristics of tumours and their importance for hyperthermia: heterogeneity is the key issue. Int J Hyperthermia. 2010;26(3):211–223.
   PubMed Web of Science ®Google Scholar
• Sun X, Xing L, Ling CC, et al. The effect of mild temperature hyperthermia on tumour hypoxia and blood perfusion: relevance for radiotherapy, vascular targeting and imaging. Int J Hyperthermia. 2010;26(3):224–231.
   PubMed Web of Science ®Google Scholar
• Elming PB, Sorensen BS, Oei AL, Franken NAP, et al. Hyperthermia: the optimal treatment to overcome radiation resistant hypoxia. Cancers (Basel). 2019;11(1):60.
   PubMed Web of Science ®Google Scholar
• Leith JT, Miller RC, Gerner EW, et al. Hyperthermic potentiation: biological aspects and applications to radiation therapy. Cancer. 1977;39(S2):766–779.
   PubMed Web of Science ®Google Scholar
• Connor WG, Gerner EW, Miller RC, et al. Prospects for hyperthermia in human cancer therapy. Part II: implications of biological and physical data for applications of hyperthermia to man. Radiology. 1977;123(2):497–503.
   PubMed Web of Science ®Google Scholar
• Gerner EW, Leith JT. Interaction of hyperthermia with radiations of different linerar energy transfer. Int J Radiat Biol Relat Stud Phys Chem Med. 1977;31(3):283–288.
   PubMed Web of Science ®Google Scholar
• Gerner EW, Leith JT, Boone ML. Mammalian cell survival response following irradiation with 4 MeV X rays or accelerated helium ions combined with hyperthermia. Radiology. 1976;119(3):715–720.
   PubMed Web of Science ®Google Scholar
• Maeda J, Fujii Y, Fujisawa H, et al. Hyperthermia-induced radiosensitization in CHO wild-type, NHEJ repair mutant and HR repair mutant following proton and carbon-ion exposure. Oncol Lett. 2015;10(5):2828–2834.
   PubMed Web of Science ®Google Scholar
• Franken NA, Oei AL, Kok HP, et al. Cell survival and radiosensitisation: modulation of the linear and quadratic parameters of the LQ model (Review). Int J Oncol. 2013;42(5):1501–1515.
   PubMed Web of Science ®Google Scholar
• Oei AL, Vriend LE, Crezee J, et al. Effects of hyperthermia on DNA repair pathways: one treatment to inhibit them all. Radiat Oncol. 2015;10(1):165.
   PubMed Web of Science ®Google Scholar
• Furusawa Y, Fukutsu K, Aoki M, 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(5):485–496.2.0.CO;2]
   PubMed Web of Science ®Google Scholar
• Hahn EW, Canada TR, Alfieri AA, et al. The interaction of hyperthermia with fast neutrons or x rays on local tumor response. Radiat Res. 1976;68(1):39–56.
   PubMed Web of Science ®Google Scholar
• van der Zee J, Gonzalez Gonzalez D, van Rhoon GC, et al. Comparison of radiotherapy alone with radiotherapy plus hyperthermia in locally advanced pelvic tumours: a prospective, randomised, multicentre trial. Dutch Deep Hyperthermia Group. Lancet. 2000;355(9210):1119–1125.
   PubMed Web of Science ®Google Scholar
• Wust P, Hildebrandt B, Sreenivasa G, et al. Hyperthermia in combined treatment of cancer. Lancet Oncol. 2002;3(8):487–497.
   PubMed Web of Science ®Google Scholar
• Datta NR, Stutz E, Puric E, et al. A pilot study of radiotherapy and local hyperthermia in elderly patients with muscle-invasive bladder cancers unfit for definitive surgery or chemoradiotherapy. Front Oncol. 2019;9:889.
   PubMed Web of Science ®Google Scholar
• Maluta S, Dall’oglio S, Romano M, et al. Conformal radiotherapy plus local hyperthermia in patients affected by locally advanced high risk prostate cancer: preliminary results of a prospective phase II study. Int J Hyperthermia. 2007;23(5):451–456.
   PubMed Web of Science ®Google Scholar
• Vernon CC, Hand JW, Field SB, 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. Int J Radiat Oncol Biol Phys. 1996;35:731–744.
   PubMed Web of Science ®Google Scholar
• Datta NR, Schneider R, Puric E, et al. Proton irradiation with hyperthermia in unresectable soft tissue sarcoma. Int J Particle Ther. 2016;3(2):327–336.
   PubMedGoogle Scholar
• Tran S, Puric E, Walser M, et al. Early results and volumetric analysis after spot-scanning proton therapy with concomitant hyperthermia in large inoperable sacral chordomas. Br J Radiol. 2019;92:20180883.
   Web of Science ®Google Scholar
• Overgaard J, Gonzalez Gonzalez D, Hulshof MC, et al. Randomised trial of hyperthermia as adjuvant to radiotherapy for recurrent or metastatic malignant melanoma. European society for hyperthermic oncology. Lancet. 1995;345(8949):540–543.
   PubMed Web of Science ®Google Scholar
• Dewhirst MW, Sim DA. The utility of thermal dose as a predictor of tumor and normal tissue responses to combined radiation and hyperthermia. Cancer Res. 1984;44(10):4772s–4780s.
   PubMed Web of Science ®Google Scholar
• Emami B, Scott C, Perez CA, et al. Phase III study of interstitial thermoradiotherapy compared with interstitial radiotherapy alone in the treatment of recurrent or persistent human tumors. A prospectively controlled randomized study by the Radiation Therapy Group. Int J Radiat Oncol Biol Phys. 1996;34(5):1097–1104.
   PubMed Web of Science ®Google Scholar