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Reviews

Biological modeling in thermoradiotherapy: present status and ongoing developments toward routine clinical use

ORCID Icon, ORCID Icon, , ORCID Icon & ORCID Icon
Pages 1126-1140 | Received 07 Jun 2022, Accepted 11 Aug 2022, Published online: 23 Aug 2022

References

  • Sanchez-Nieto B, Nahum AE. BIOPLAN: software for the biological evaluation of radiotherapy treatment plans. Med Dosim. 2000;25(2):71–76.
  • Sanchez-Nieto B, Nahum AE. The Delta-TCP concept: a clinically useful measure of tumor control probability. Int J Radiat Oncol Biol Phys. 1999;44(2):369–380.
  • Sanchez-Nieto B, Nahum AE, Dearnaley DP. Individualization of dose prescription based on normal-tissue dose-volume and radiosensitivity data. Int J Radiat Oncol Biol Phys. 2001;49(2):487–499.
  • Jones B, Dale RG, Deehan C, et al. The role of biologically effective dose (BED) in clinical oncology. Clin Oncol. 2001;13(2):71–81.
  • Stavrev PV, Stavreva N, Ruggieri R, et al. Theoretical investigation of the impact of different timing schemes in hypofractionated radiotherapy. Med Phys. 2021;48(7):4085–4098.
  • Peeken JC, Vaupel P, Combs SE. Integrating hyperthermia into modern radiation oncology: what evidence is necessary? Front Oncol. 2017;7:132.
  • Datta NR, Kok HP, Crezee H, et al. Integrating loco-regional hyperthermia Into the current oncology practice: SWOT and TOWS analyses. Front Oncol. 2020;10(819):819.
  • Kampinga HH, Dikomey E. Hyperthermic radiosensitization: mode of action and clinical relevance. Int J Radiat Biol. 2001;77(4):399–408.
  • Repasky EA, Evans SS, Dewhirst MW. Temperature matters! And why it should matter to tumor immunologists. Cancer Immunol Res. 2013;1(4):210–216.
  • van Rhoon GC. Is CEM43 still a relevant thermal dose parameter for hyperthermia treatment monitoring? Int J Hyperth. 2016;32(1):50–62.
  • Bakker A, Tello Valverde CP, van Tienhoven G, et al. Post-operative re-irradiation with hyperthermia in locoregional breast cancer recurrence: temperature matters. Radiother Oncol. 2022;167:149–157.
  • Bakker A, Van der Zee J, van tienhoven G, et al. Temperature and thermal dose during radiotherapy and hyperthermia for recurrent breast cancer are related to clinical outcome and thermal toxicity: a systematic review. Int J Hyperth. 2019;36(1):1024–1039.
  • Kroesen M, Mulder HT, Van Holthe JML, et al. Confirmation of thermal dose as a predictor of local control in cervical carcinoma patients treated with state-of-the-art radiation therapy and hyperthermia. Radiother Oncol. 2019;140:150–158.
  • Rau B, Wust P, Tilly W, et al. Preoperative radiochemotherapy in locally advanced or recurrent rectal cancer: regional radiofrequency hyperthermia correlates with clinical parameters. Int J Radiat Oncol Biol Phys. 2000;48(2):381–391.
  • Overgaard J, Gonzalez DG, Hulshof MCCH, et al. Hyperthermia as an adjuvant to radiation therapy of recurrent or metastatic malignant melanoma. A multicentre randomized trial by the European Society for Hyperthermic Oncology. Int J Hyperth. 1996;12(1):3–20.
  • Ohguri T, Harima Y, Imada H, et al. Relationships between thermal dose parameters and the efficacy of definitive chemoradiotherapy plus regional hyperthermia in the treatment of locally advanced cervical cancer: data from a multicentre randomised clinical trial. Int J Hyperth. 2018;34(4):461–468.
  • Franckena M, Fatehi D, de Bruijne M, et al. Hyperthermia dose-effect relationship in 420 patients with cervical cancer treated with combined radiotherapy and hyperthermia. Eur J Cancer. 2009;45(11):1969–1978.
  • Sapareto SA, Dewey WC. Thermal dose determination in cancer therapy. Int J Radiat Oncol Biol Phys. 1984;10(6):787–800.
  • de Bruijne M, van der Holt B, van Rhoon GC, et al. Evaluation of CEM43 degrees CT90 thermal dose in superficial hyperthermia: a retrospective analysis. Strahlenther Onkol. 2010;186(8):436–443.
  • Overgaard J. Simultaneous and sequential hyperthermia and radiation treatment of an experimental tumor and its surrounding normal tissue in vivo. Int J Radiat Oncol Biol Phys. 1980;6(11):1507–1517.
  • Issels R, Kampmann E, Kanaar R, et al. Hallmarks of hyperthermia in driving the future of clinical hyperthermia as targeted therapy: translation into clinical application. Int J Hyperth. 2016;32(1):89–95.
  • Gerweck LE, Nygaard TG, Burlett M. Response of cells to hyperthermia under acute and chronic hypoxic conditions. Cancer Res. 1979;39(3):966–972.
  • Suit HD, Gerweck LE. Potential for hyperthermia and radiation therapy. Cancer Res. 1979;39(6 Pt 2):2290–2298.
  • Kampinga HH. Cell biological effects of hyperthermia alone or combined with radiation or drugs: a short introduction to newcomers in the field. Int J Hyperth. 2006;22(3):191–196.
  • Ihara M, Takeshita S, Okaichi K, et al. Heat exposure enhances radiosensitivity by depressing DNA-PK kinase activity during double strand break repair. Int J Hyperth. 2014;30(2):102–109.
  • Krawczyk PM, Eppink B, Essers J, et al. Mild hyperthermia inhibits homologous recombination, induces BRCA2 degradation, and sensitizes cancer cells to poly (ADP-ribose) polymerase-1 inhibition. Proc Natl Acad Sci USA. 2011;108(24):9851–9856.
  • van den Tempel N, Laffeber C, Odijk H, et al. The effect of thermal dose on hyperthermia-mediated inhibition of DNA repair through homologous recombination. Oncotarget. 2017;8(27):44593–44604.
  • Van Leeuwen CM, Oei AL, Chin KWTK, et al. A short time interval between radiotherapy and hyperthermia reduces in-field recurrence and mortality in women with advanced cervical cancer. Radiat Oncol. 2017;12(1):75.
  • Bader SB, Dewhirst MW, Hammond EM. Cyclic hypoxia: an update on its characteristics, methods to measure it and biological implications in cancer. Cancers. 2020;13(1):23.
  • Vujaskovic Z, Song CW. Physiological mechanisms underlying heat-induced radiosensitization. Int J Hyperth. 2004;20(2):163–174.
  • Winslow TB, Eranki A, Ullas S, et al. A pilot study of the effects of mild systemic heating on human head and neck tumour xenografts: analysis of tumour perfusion, interstitial fluid pressure, hypoxia and efficacy of radiation therapy. Int J Hyperth. 2015;31(6):693–701.
  • Song CW, Shakil A, Osborn JL, et al. Tumour oxygenation is increased by hyperthermia at mild temperatures. Int J Hyperth. 1996;12(3):367–373.
  • Song CW. Effect of local hyperthermia on blood flow and microenvironment: a review. Cancer Res. 1984;44(10 Suppl):4721s–4730s.
  • Dewhirst MW, Vujaskovic Z, Jones E, et al. Re-setting the biologic rationale for thermal therapy. Int J Hyperth. 2005;21(8):779–790.
  • Dewhirst MW, Oleson JR, Kirkpatrick J, et al. Accurate three-dimensional thermal dosimetry and assessment of physiologic response are essential for optimizing thermoradiotherapy. Cancers. 2022;14(7):1701.
  • Toraya-Brown S, Fiering S. Local tumour hyperthermia as immunotherapy for metastatic cancer. Int J Hyperth. 2014;30(8):531–539.
  • Multhoff G, Hightower LE. Cell surface expression of heat shock proteins and the immune response. Cell Stress Chaper. 1996;1(3):167–176.
  • 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.
  • 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.
  • Fisher DT, Chen Q, Skitzki JJ, et al. IL-6 trans-signaling licenses mouse and human tumor microvascular gateways for trafficking of cytotoxic T cells. J Clin Invest. 2011;121(10):3846–3859.
  • Seynhaeve ALB, Amin M, Haemmerich D, et al. Hyperthermia and smart drug delivery systems for solid tumor therapy. Adv Drug Deliv Rev. 2020;163-164:125–144.
  • Werthmoller N, Frey B, Ruckert M, et al. Combination of ionising radiation with hyperthermia increases the immunogenic potential of B16-F10 melanoma cells in vitro and in vivo. Int J Hyperth. 2016;32(1):23–30.
  • Ruckert M, Deloch L, Fietkau R, et al. Immune modulatory effects of radiotherapy as basis for well-reasoned radioimmunotherapies. Strahlenther Onkol. 2018;194(6):509–519.
  • Adnan A, Munoz NM, Prakash P, et al. Hyperthermia and tumor immunity. Cancers. 2021;13(11):2507.
  • Bull JMC. A review of immune therapy in cancer and a question: can thermal therapy increase tumor response? Int J Hyperth. 2018;34(6):840–852.
  • Hader M, Frey B, Fietkau R, et al. Immune biological rationales for the design of combined radio- and immunotherapies. Cancer Immunol Immunother. 2020;69(2):293–306.
  • Mahmood J, Shukla HD, Soman S, et al. Immunotherapy, radiotherapy, and hyperthermia: a combined therapeutic approach in pancreatic cancer treatment. Cancers. 2018;10(12):469.
  • Hurwitz MD. Hyperthermia and immunotherapy: clinical opportunities. Int J Hyperth. 2019;36(sup1):4–9.
  • Sengedorj A, Hader M, Heger L, et al. The effect of hyperthermia and radiotherapy sequence on cancer cell death and the immune phenotype of breast cancer cells. Cancers. 2022;14(9):2050.
  • Deckers R, Debeissat C, Fortin PY, et al. Arrhenius analysis of the relationship between hyperthermia and Hsp70 promoter activation: a comparison between ex vivo and in vivo data. Int J Hyperth. 2012;28(5):441–450.
  • Moritz AR, Henriques FC. Studies of thermal injury: II. The relative importance of time and surface temperature in the causation of cutaneous burns. Am J Pathol. 1947;23(5):695–720.
  • Pearce JA. Comparative analysis of mathematical models of cell death and thermal damage processes. Int J Hyperth. 2013;29(4):262–280.
  • Jung H. A generalized concept for cell killing by heat. Radiat Res. 1986;106(1):56–72.
  • Roizin-Towle L, Pirro JP. The response of human and rodent cells to hyperthermia. Int J Radiat Oncol Biol Phys. 1991;20(4):751–756.
  • Jung H. A generalized concept for cell killing by heat. Effect of chronically induced thermotolerance. Radiat Res. 1991;127(3):235–242.
  • Roti JL, Henle KJ. Comparison of two mathematical models for describing heat-induced cell killing. Radiat Res. 1980;81(3):374–383.
  • Scheidegger S, Fuchs HU, Zaugg K, et al. Using state variables to model the response of tumour cells to radiation and heat: a novel multi-hit-repair approach. Comput Math Methods Med. 2013;2013:587543.
  • Weyland MS, Thumser-Henner P, Nytko KJ, et al. Holistic view on cell survival and DNA damage: how model-based data analysis supports exploration of dynamics in biological systems. Comput Math Methods Med. 2020;2020:5972594.
  • Scheidegger S, Barba SM, Gaipl US. Theoretical evaluation of the impact of hyperthermia in combination with radiation therapy in an artificial immune-tumor-ecosystem. Cancers. 2021;13(22):5764.
  • Fowler JF. The linear-quadratic formula and progress in fractionated radiotherapy. Br J Radiol. 1989;62(740):679–694.
  • McMahon SJ. The linear quadratic model: usage, interpretation and challenges. Phys Med Biol. 2018;64(1):01TR01.
  • Fowler JF. Development of radiobiology for oncology-a personal view. Phys Med Biol. 2006;51(13):R263–86.
  • Myerson RJ, Roti Roti JL, Moros EG, et al. Modelling heat-induced radiosensitization: clinical implications. Int J Hyperth. 2004;20(2):201–212.
  • Xu M, Myerson RJ, Straube WL, et al. Radiosensitization of heat resistant human tumour cells by 1 hour at 41.1 degrees C and its effect on DNA repair. Int J Hyperth. 2002;18(5):385–403.
  • 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.
  • 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.
  • Van Leeuwen CM, Oei AL, Ten Cate R, et al. Measurement and analysis of the impact of time-interval, temperature and radiation dose on tumour cell survival and its application in thermoradiotherapy plan evaluation. Int J Hyperth. 2018;34(1):30–38.
  • Bruningk SC, Ijaz J, Rivens I, et al. A comprehensive model for heat-induced radio-sensitisation. Int J Hyperth. 2018;34(4):392–402.
  • Powathil GG, Adamson DJA, Chaplain MAJ. Towards predicting the response of a solid tumour to chemotherapy and radiotherapy treatments: clinical insights from a computational model. PLOS Comput Biol. 2013;9(7):e1003120.
  • Powathil GG, Swat M, Chaplain MAJ. Systems oncology: towards patient-specific treatment regimes informed by multiscale mathematical modelling. Semin Cancer Biol. 2015;30:13–20.
  • Bruningk S, Powathil G, Ziegenhein P, et al. Combining radiation with hyperthermia: a multiscale model informed by in vitro experiments. J R Soc Interface. 2018;15(138):20170681.
  • De Mendoza AM, Michlikova S, Berger J, et al. Mathematical model for the thermal enhancement of radiation response: thermodynamic approach. Sci Rep. 2021;11(1):5503.
  • Kok HP, Crezee J, Franken NAP, et al. Quantifying the combined effect of radiation therapy and hyperthermia in terms of equivalent dose distributions. Int J Radiat Oncol Biol Phys. 2014;88(3):739–745.
  • van Leeuwen CM, Crezee J, Oei AL, et al. 3D radiobiological evaluation of combined radiotherapy and hyperthermia treatments. Int J Hyperth. 2017;33(2):160–169.
  • Crezee J, van Leeuwen CM, Oei AL, et al. Biological modelling of the radiation dose escalation effect of regional hyperthermia in cervical cancer. Radiat Oncol. 2016;11:14.
  • Kok HP, Van Dijk I, Crama KF, et al. Reirradiation plus hyperthermia for recurrent pediatric sarcoma; a simulation study to investigate feasibility. Int J Oncol. 2019;54(1):209–218.
  • Le Guevelou J, Chirila ME, Achard V, et al. Combined hyperthermia and radiotherapy for prostate cancer: a systematic review. Int J Hyperth. 2022;39(1):547–556.
  • Beck M, Ghadjar P, Mehrhof F, et al. Salvage-Radiation therapy and regional hyperthermia for biochemically recurrent prostate cancer after radical prostatectomy (results of the planned interim analysis). Cancers. 2021;13(5):1133.
  • van Leeuwen CM, Crezee J, Oei AL, et al. The effect of time interval between radiotherapy and hyperthermia on planned equivalent radiation dose. Int J Hyperth. 2018;34(7):901–909.
  • Kroesen M, Mulder HT, van Holthe JML, et al. The effect of the time interval Between radiation and hyperthermia on clinical outcome in 400 locally advanced cervical carcinoma patients. Front Oncol. 2019;9:134.
  • Crezee J, Oei AL, Franken NAP, et al. Response: commentary: the impact of the time interval Between radiation and hyperthermia on clinical outcome in patients with locally advanced cervical cancer. Front Oncol. 2020;10(528):528.
  • Crezee H, Kok HP, Oei AL, et al. The impact of the time interval between radiation and hyperthermia on clinical outcome in patients with locally advanced cervical cancer. Front Oncol. 2019;9:412.
  • Kroesen M, Mulder HT, van Rhoon GC, et al. Commentary: the impact of the time interval between radiation and hyperthermia on clinical outcome in patients with locally advanced cervical cancer. Front Oncol. 2019;9:1387.
  • Ghaderi Aram M, Zanoli M, Nordstrom H, et al. Radiobiological evaluation of combined gamma knife radiosurgery and hyperthermia for pediatric neuro-oncology. Cancers. 2021;13(13):3277.
  • Schooneveldt G, Dobsicek Trefna H, Persson M, et al. Hyperthermia treatment planning including convective flow in cerebrospinal fluid for brain tumour hyperthermia treatment using a novel dedicated paediatric brain applicator. Cancers. 2019;11(8):1183.
  • Androulakis I, Mestrom RMC, Christianen M, et al. A novel framework for the optimization of simultaneous ThermoBrachyTherapy. Cancers. 2022;14(6):1425.
  • Bruggmoser G, Bauchowitz S, Canters R, et al. Quality assurance for clinical studies in regional deep hyperthermia. Strahlenther Onkol. 2011;187(10):605–610.
  • Trefna HD, Crezee H, Schmidt M, et al. Quality assurance guidelines for superficial hyperthermia clinical trials: I. Clinical requirements. Int J Hyperth. 2017;33(4):471–482.
  • Brenner DJ, Hlatky LR, Hahnfeldt PJ, et al. A convenient extension of the linear-quadratic model to include redistribution and reoxygenation. Int J Radiat Oncol Biol Phys. 1995;32(2):379–390.
  • Nahum AE, Movsas B, Horwitz EM, et al. Incorporating clinical measurements of hypoxia into tumor local control modeling of prostate cancer: implications for the alpha/beta ratio. Int J Radiat Oncol Biol Phys. 2003;57(2):391–401.
  • Niendorf T, Pohlmann A, Arakelyan K, et al. How bold is blood oxygenation level-dependent (BOLD) magnetic resonance imaging of the kidney? Opportunities, challenges and future directions. Acta Physiol. 2015;213(1):19–38.
  • Wijsman R, Kaanders JH, Oyen WJ, et al. Hypoxia and tumor metabolism in radiation oncology: targets visualized by positron emission tomography. Q J Nucl Med Mol Imaging. 2013;57(3):244–256.
  • Myerson RJ, Singh AK, Bigott HM, et al. Monitoring the effect of mild hyperthermia on tumour hypoxia by Cu-ATSM PET scanning. Int J Hyperth. 2006;22(2):93–115.
  • Hsieh CH, Lee CH, Liang JA, et al. Cycling hypoxia increases U87 glioma cell radioresistance via ROS induced higher and long-term HIF-1 signal transduction activity. Oncol Rep. 2010;24(6):1629–1636.
  • Moon EJ, Sonveaux P, Porporato PE, et al. NADPH oxidase-mediated reactive oxygen species production activates hypoxia-inducible factor-1 (HIF-1) via the ERK pathway after hyperthermia treatment. Proc Natl Acad Sci USA. 2010;107(47):20477–20482.
  • Vaupel PW, Kelleher DK. Pathophysiological and vascular characteristics of tumours and their importance for hyperthermia: heterogeneity is the key issue. Int J Hyperth. 2010;26(3):211–223.
  • Horsman MR, Overgaard J. Can mild hyperthermia improve tumour oxygenation? Int J Hyperth. 1997;13(2):141–147.
  • Gellermann J, Hildebrandt B, Issels R, et al. Noninvasive magnetic resonance thermography of soft tissue sarcomas during regional hyperthermia: correlation with response and direct thermometry. Cancer. 2006;107(6):1373–1382.
  • Boehm C, Goeger-Neff M, Mulder HT, et al. Susceptibility artifact correction in MR thermometry for monitoring of mild radiofrequency hyperthermia using total field inversion. Magn Reson Med. 2022;88(1):120–132.
  • Kok HP, Van den Berg CAT, Bel A, et al. Fast thermal simulations and temperature optimization for hyperthermia treatment planning, including realistic 3D vessel networks. Med Phys. 2013;40(10):103303.
  • Kotte AN, van Leeuwen GM, Lagendijk JJ. Modelling the thermal impact of a discrete vessel tree. Phys Med Biol. 1999;44(1):57–74.
  • Kok HP, Crezee J. Adapt2Heat: treatment planning-assisted locoregional hyperthermia by on-line visualization, optimization and re-optimization of SAR and temperature distributions. Int J Hyperth. 2022;39(1):265–277.
  • Kok HP, Korshuize - van Straten L, Bakker A, et al. On-line adaptive hyperthermia treatment planning during locoregional heating to suppress treatment limiting hot spots. Int J Radiat Oncol Biol Phys. 2017;99(4):1039–1047.
  • Datta NR, Puric E, Schneider R, et al. Could hyperthermia with proton therapy mimic carbon ion therapy? Exploring a thermo-radiobiological rationale. Int J Hyperth. 2014;30(7):524–530.
  • Franken NA, Barendsen GW. Enhancement of radiation effectiveness by hyperthermia and incorporation of halogenated pyrimidines at low radiation doses as compared with high doses: implications for mechanisms. Int J Radiat Biol. 2014;90(4):313–317.
  • Eppink B, Krawczyk PM, Stap J, et al. Hyperthermia-induced DNA repair deficiency suggests novel therapeutic anti-cancer strategies. Int J Hyperth. 2012;28(6):509–517.
  • Plataniotis GA, Dale RG. Use of concept of chemotherapy-equivalent biologically effective dose to provide quantitative evaluation of contribution of chemotherapy to local tumor control in chemoradiotherapy cervical cancer trials. Int J Radiat Oncol Biol Phys. 2008;72(5):1538–1543.
  • Crezee J, Barendsen GW, Westermann AM, et al. Quantification of the contribution of hyperthermia to results of cervical cancer trials: in regard to plataniotis and dale (int J radiat oncol biol phys 2009;73:1538-1544). Int J Radiat Oncol Biol Phys. 2009;75(2):634–635.