No retraction, correction or concern found when last checked on Oct 20, 2026.

Carbon Ion Radiobiology

Walter Tinganelli, Marco Durante

Cancers · 2020 · Review · CC BY

doi:10.20944/preprints202010.0055.v1

Abstract

Simple Summary. Radiotherapy with carbon ions has been used for over 20 years in Asia and Europe and is now planned in the USA. The physics advantages of carbon ions compared to X-rays are similar to those of protons, but their radiobiological features are quite distinct and may lead to a breakthrough in the treatment of some cancers characterized by high mortality.

Abstract. Radiotherapy using accelerated charged particles is rapidly growing worldwide. About 85% of the cancer patients receiving particle therapy are irradiated with protons, which have physical advantages compared to X-rays but a similar biological response. In addition to the ballistic advantages, heavy ions present specific radiobiological features that can make them attractive for treating radioresistant, hypoxic tumors. An ideal heavy ion should have lower toxicity in the entrance channel (normal tissue) and be exquisitely effective in the target region (tumor). Carbon ions have been chosen because they represent the best combination in this direction. Normal tissue toxicities and second cancer risk are similar to those observed in conventional radiotherapy. In the target region, they have increased relative biological effectiveness and a reduced oxygen enhancement ratio compared to X-rays. Some radiobiological properties of densely ionizing carbon ions are so distinct from X-rays and protons that they can be considered as a different “drug” in oncology, and may elicit favorable responses such as an increased immune response and reduced angiogenesis and metastatic potential. The radiobiological properties of carbon ions should guide patient selection and treatment protocols to achieve optimal clinical results.

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Novel stereotactic body radiation therapy (SBRT)-based partial tumor irradiation targeting hypoxic segment of bulky tumors (SBRT-PATHY): improvement of the radiotherapy outcome by exploiting the bystander and abscopal effects · 2019
Not checked
95.
Emami B. Tolerance of Normal Tissue to Therapeutic Radiation. Rep. Radiother. Oncol. 2013;1:123-127.
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96.
Friedrich T., Scholz U., Durante M., Scholz M. RBE of ion beams in hypofractionated radiotherapy (SBRT). Phys. Med. 2014;30:588-591.
Not in our library10.1016/j.ejmp.2014.04.009
97.
Chapman J.D. Can the two mechanisms of tumor cell killing by radiation be exploited for therapeutic gain? J. Radiat. Res. 2014;55:2-9.
Not in our library10.1093/jrr/rrt111
98.
Jeong J., Taasti V.T., Jackson A., Deasy J.O. The Relative Biological Effectiveness of Carbon Ion Radiation Therapy for Early Stage Lung Cancer. Radiother. Oncol. 2020.
Not in our library10.1016/j.radonc.2020.09.027
99.
Saager M., Glowa C., Peschke P., Brons S., Gr?n R., Scholz M., Huber P.E., Debus J., Karger C.P. The relative biological effectiveness of carbon ion irradiations of the rat spinal cord increases linearly with LET up to 99 keV/micron. Acta Oncol. (Madr.). 2016;55:1512-1515.
Not in our library10.1080/0284186x.2016.1250947
100.
Saager M., Glowa C., Peschke P., Brons S., Scholz M., Huber P.E., Debus J., Karger C.P. Carbon Ion Irradiation of the Rat Spinal Cord: Dependence of the Relative Biological Effectiveness on Linear Energy Transfer. Int. J. Radiat. Oncol. Biol. Phys. 2014;90:63-70.
Not in our library10.1016/j.ijrobp.2014.05.008
101.
Fractionated carbon ion irradiations of the rat spinal cord: comparison of the relative biological effectiveness with predictions of the local effect model · 2020
Not checked
102.
Karger C.P., Peschke P., Sanchez-Brandelik R., Scholz M., Debus J. Radiation tolerance of the rat spinal cord after 6 and 18 fractions of photons and carbon ions: Experimental results and clinical implications. Int. J. Radiat. Oncol. 2006;66:1488-1497.
Not in our library10.1016/j.ijrobp.2006.08.045
103.
Saager M., Glowa C., Peschke P., Brons S., Grün R., Scholz M., Huber P.E., Debus J., Karger C.P. Split dose carbon ion irradiation of the rat spinal cord: Dependence of the relative biological effectiveness on dose and linear energy transfer. Radiother. Oncol. 2015;117:358-363.
Not in our library10.1016/j.radonc.2015.07.006
104.
Saager M., Peschke P., Welzel T., Huang L., Brons S., Grün R., Scholz M., Debus J., Karger C.P. Late normal tissue response in the rat spinal cord after carbon ion irradiation. Radiat. Oncol. 2018;13:5.
Not in our library10.1186/s13014-017-0950-5
105.
Ando K., Koike S., Uzawa A., Takai N., Fukawa T., Furusawa Y., Aoki M., Miyato Y. Biological Gain of Carbon-ion Radiotherapy for the Early Response of Tumor Growth Delay and against Early Response of Skin Reaction in Mice. J. Radiat. Res. 2005;46:51-57.
Not in our library10.1269/jrr.46.51
106.
Sørensen B.S., Horsman M.R., Alsner J., Overgaard J., Durante M., Scholz M., Friedrich T., Bassler N. Relative biological effectiveness of carbon ions for tumor control, acute skin damage and late radiation-induced fibrosis in a mouse model. Acta Oncol. (Madr.). 2015;54:1623-1630.
Not in our library10.3109/0284186x.2015.1069890
107.
Glowa C., Karger C.P., Brons S., Zhao D., Mason R.P., Huber P.E., Debus J., Peschke P. Carbon ion radiotherapy decreases the impact of tumor heterogeneity on radiation response in experimental prostate tumors. Cancer Lett. 2016;378:97-103.
Not in our library10.1016/j.canlet.2016.05.013
108.
Glowa C., Peschke P., Brons S., Debus J., Karger C.P. Intrinsic and extrinsic tumor characteristics are of minor relevance for the efficacy of split-dose carbon ion irradiation in three experimental prostate tumors. Radiother. Oncol. 2019;133:120-124.
Not in our library10.1016/j.radonc.2018.12.017
109.
Glowa C., Peschke P., Brons S., Neels O.C., Kopka K., Debus J., Karger C.P. Carbon ion radiotherapy: Impact of tumor differentiation on local control in experimental prostate carcinomas. Radiat. Oncol. 2017;12:174.
Not in our library10.1186/s13014-017-0914-9
110.
Bert C., Engenhart-Cabillic R., Durante M. Particle therapy for noncancer diseases. Med. Phys. 2012;39:1716-1727.
Not in our library10.1118/1.3691903
111.
van der Ree M.H., Blanck O., Limpens J., Lee C.H., Balgobind B.V., Dieleman E.M.T., Wilde A.A.M., Zei P.C., de Groot J.R., Slotman B.J., et al. Cardiac radioablation—A systematic review. Heart Rhythm. 2020;17:1381-1392.
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112.
Cuculich P.S., Schill M.R., Kashani R., Mutic S., Lang A., Cooper D., Faddis M., Gleva M., Noheria A., Smith T.W., et al. Noninvasive Cardiac Radiation for Ablation of Ventricular Tachycardia. N. Engl. J. Med. 2017;377:2325-2336.
Not in our library10.1056/nejmoa1613773
113.
Lehmann H.I., Graeff C., Simoniello P., Constantinescu A., Takami M., Lugenbiel P., Richter D., Eichhorn A., Prall M., Kaderka R., et al. Feasibility Study on Cardiac Arrhythmia Ablation Using High-Energy Heavy Ion Beams. Sci. Rep. 2016;6:38895.
Not in our library10.1038/srep38895
114.
Rapp F., Simoniello P., Wiedemann J., Bahrami K., Grünebaum V., Ktitareva S., Durante M., Lugenbiel P., Thomas D., Lehmann H.I., et al. Biological Cardiac Tissue Effects of High-Energy Heavy Ions – Investigation for Myocardial Ablation. Sci. Rep. 2019;9:5000.
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115.
Uzawa A., Ando K., Kase Y., Hirayama R., Matsumoto Y., Matsufuji N., Koike S., Kobashi G. Designing a ridge filter based on a mouse foot skin reaction to spread out Bragg-peaks for carbon-ion radiotherapy. Radiother. Oncol. 2015;115:279-283.
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116.
Ando S., Koike K., Nojima Y.-J., Chen C.K. Mouse skin reactions following fractionated irradiation with carbon ions. Int. J. Radiat. Biol. 1998;74:129-138.
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117.
Kagawa K., Murakami M., Hishikawa Y., Abe M., Akagi T., Yanou T., Kagiya G., Furusawa Y., Ando K., Nojima K., et al. Preclinical biological assessment of proton and carbon ion beams at Hyogo Ion Beam Medical Center. Int. J. Radiat. Oncol. 2002;54:928-938.
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118.
Raju M.R., Carpenter S.G. A heavy particle comparative study. Part IV: Acute and late reactions. Br. J. Radiol. 1978;51:720-727.
Not in our library10.1259/0007-1285-51-609-720
119.
Zhou C., Jones B., Moustafa M., Yang B., Brons S., Cao L., Dai Y., Schwager C., Chen M., Jaekel O., et al. Determining RBE for development of lung fibrosis induced by fractionated irradiation with carbon ions utilizing fibrosis index and high-LET BED model. Clin. Transl. Radiat. Oncol. 2019;14:25-32.
Not in our library10.1016/j.ctro.2018.10.005
120.
Zhou C., Jones B., Moustafa M., Schwager C., Bauer J., Yang B., Cao L., Jia M., Mairani A., Chen M., et al. Quantitative assessment of radiation dose and fractionation effects on normal tissue by utilizing a novel lung fibrosis index model. Radiat. Oncol. 2017;12:172.
Not in our library10.1186/s13014-017-0912-y
121.
Brownstein J.M., Wisdom A.J., Castle K.D., Mowery Y.M., Guida P., Lee C., Durante M., Kirsch D.G. Characterizing the Potency and Impact of Carbon Ion Therapy in a Primary Mouse Model of Soft Tissue Sarcoma. Mol. Cancer Ther. 2018;17:858-868.
Not in our library10.1158/1535-7163.mct-17-0965
122.
Koike S., Ando K., Oohira C., Fukawa T., Lee R., Takai N., Monobe M., Furusawa Y., Aoki M., Yamada S., et al. Relative Biological Effectiveness of 290 MeV/u Carbon Ions for the Growth Delay of a Radioresistant Murine Fibrosarcoma. J. Radiat. Res. 2002;43:247-255.
Not in our library10.1269/jrr.43.247
123.
Yoshida Y., Ando K., Ando K., Murata K., Yoshimoto Y., Musha A., Kubo N., Kawamura H., Koike S., Uzawa A., et al. Evaluation of therapeutic gain for fractionated carbon-ion radiotherapy using the tumor growth delay and crypt survival assays. Radiother. Oncol. 2015;117:351-357.
Not in our library10.1016/j.radonc.2015.09.027
124.
Takahashi A., Yano T., Matsumoto H., Wang X., Ohnishi K., Tamamoto T., Tsuji K., Yukawa O., Ohnishi T. Effects of accelerated carbon-ions on growth inhibition of transplantable human esophageal cancer in nude mice. Cancer Lett. 1998;122:181-186.
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125.
Peschke P., Karger C.P., Scholz M., Debus J., Huber P.E. Relative Biological Effectiveness of Carbon Ions for Local Tumor Control of a Radioresistant Prostate Carcinoma in the Rat. Int. J. Radiat. Oncol. 2011;79:239-246.
Not in our library10.1016/j.ijrobp.2010.07.1976
126.
Schmid T.E., Multhoff G., Guckenberger M., Combs S.E., Zips D. Preclinical Mouse Models for the Evaluation of Novel Techniques in Particle Therapy. Advances in Radiation Therapy. 2018;122-129.
Not in our library10.1159/000486999
127.
Hagiwara Y., Bhattacharyya T., Matsufuji N., Isozaki Y., Takiyama H., Nemoto K., Tsuji H., Yamada S. Influence of dose-averaged linear energy transfer on tumour control after carbon-ion radiation therapy for pancreatic cancer. Clin. Transl. Radiat. Oncol. 2020;21:19-24.
Not in our library10.1016/j.ctro.2019.11.002
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Bassler N., Toftegaard J., Lühr A., Sørensen B.S., Scifoni E., Krämer M., Jäkel O., Mortensen L.S., Overgaard J., Petersen J.B. LET-painting increases tumour control probability in hypoxic tumours. Acta Oncol. 2014;53:25-32.
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Bassler N., Jäkel O., Søndergaard C.S., Petersen J.B. Dose- and LET-painting with particle therapy. Acta Oncol. 2010;49:1170-1176.
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130.
Kopp B., Mein S., Dokic I., Harrabi S., Böhlen T.T., Haberer T., Debus J., Abdollahi A., Mairani A. Development and Validation of Single Field Multi-Ion Particle Therapy Treatments. Int. J. Radiat. Oncol. Biol. Phys. 2020;106:194-205.
Not in our library10.1016/j.ijrobp.2019.10.008
131.
Sokol O., Krämer M., Hild S., Durante M., Scifoni E. Kill painting of hypoxic tumors with multiple ion beams. Phys. Med. Biol. 2019;64:045008.
Not in our library10.1088/1361-6560/aafe40
132.
Pignalosa D., Durante M. Overcoming resistance of cancer stem cells. Lancet Oncol. 2012;13:e187-e188.
Not in our library10.1016/s1470-2045(12)70196-1
133.
Bertout J.A., Patel S.A., Simon M.C. The impact of O2 availability on human cancer. Nat. Rev. Cancer. 2008;8:967-975.
Not in our library10.1038/nrc2540
134.
Bristow R.G., Hill R.P. Hypoxia and metabolism. Hypoxia, DNA repair and genetic instability. Nat. Rev. Cancer. 2008;8:180-192.
Not in our library10.1038/nrc2344
135.
Bayer C., Vaupel P. Acute versus chronic hypoxia in tumors. Strahlenther. und Onkol. 2012;188:616-627.
Not in our library10.1007/s00066-012-0085-4
136.
Acute vs. Chronic vs. Cyclic Hypoxia: Their Differential Dynamics, Molecular Mechanisms, and Effects on Tumor Progression · 2019
No notice
137.
Dewhirst M.W., Cao Y., Moeller B. Cycling hypoxia and free radicals regulate angiogenesis and radiotherapy response. Nat. Rev. Cancer. 2008;8:425-437.
Not in our library10.1038/nrc2397
138.
Barker H.E., Paget J.T.E., Khan A.A., Harrington K.J. The tumour microenvironment after radiotherapy: Mechanisms of resistance and recurrence. Nat. Rev. Cancer. 2015;15:409-425.
Not in our library10.1038/nrc3958
139.
Brown J.M., Wilson W.R. Exploiting tumour hypoxia in cancer treatment. Nat. Rev. Cancer. 2004;4:437-447.
Not in our library10.1038/nrc1367
140.
Huang J., Li J.J. Multiple Dynamics in Tumor Microenvironment Under Radiotherapy. Adv. Exp. Med. Biol. 2020;1263:175-202.
Not in our library10.1007/978-3-030-44518-8_10
141.
Pajonk F., Vlashi E., McBride W.H. Radiation resistance of cancer stem cells: The 4 R’s of radiobiology revisited. Stem Cells. 2010;28:639-648.
Not in our library10.1002/stem.318
142.
The anti-malarial atovaquone increases radiosensitivity by alleviating tumour hypoxia · 2016
No notice
143.
McGowan D.R., Skwarski M., Bradley K.M., Campo L., Fenwick J.D., Gleeson F.V., Green M., Horne A., Maughan T.S., McCole M.G., et al. Buparlisib with thoracic radiotherapy and its effect on tumour hypoxia: A phase I study in patients with advanced non-small cell lung carcinoma. Eur. J. Cancer. 2019;113:87-95.
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144.
Ashton T.M., McKenna W.G., Kunz-Schughart L.A., Higgins G.S. Oxidative Phosphorylation as an Emerging Target in Cancer Therapy. Clin. Cancer Res. 2018;24:2482-2490.
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145.
Narayanan D., Ma S., Özcelik D. Targeting the Redox Landscape in Cancer Therapy. Cancers. 2020;12:1706.
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146.
Horsman M.R., Overgaard J. The impact of hypoxia and its modification of the outcome of radiotherapy. J. Radiat. Res. 2016;57:i90-i98.
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147.
Strigari L., Benassi M., Sarnelli A., Polico R., D’Andrea M. A modified hypoxia-based TCP model to investigate the clinical outcome of stereotactic hypofractionated regimes for early stage non-small-cell lung cancer (NSCLC). Med. Phys. 2012;39:4502-4514.
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148.
Carlson D.J., Stewart R.D., Semenenko V.A. Effects of oxygen on intrinsic radiation sensitivity: A test of the relationship between aerobic and hypoxic linear-quadratic (LQ) model parameters. Med. Phys. 2006;33:3105-3115.
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Toma-Dasu I., Sandström H., Barsoum P., Dasu A. To fractionate or not to fractionate? That is the question for the radiosurgery of hypoxic tumors. J. Neurosurg. 2014;121:110-115.
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Wouters B.G., Brown J.M. Cells at intermediate oxygen levels can be more important than the “hypoxic fraction” in determining tumor response to fractionated radiotherapy. Radiat. Res. 1997;147:541-550.
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Furusawa Y., Fukutsu K., Aoki M., Itsukaichi H., Eguchi-Kasai K., Ohara H., Yatagai F., Kanai T., Ando K. 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;154:485-496.
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152.
Wenzl T., Wilkens J.J. Theoretical analysis of the dose dependence of the oxygen enhancement ratio and its relevance for clinical applications. Radiat. Oncol. 2011;6:171.
Not in our library10.1186/1748-717x-6-171
153.
McKeown S.R. Defining normoxia, physoxia and hypoxia in tumours—Implications for treatment response. Br. J. Radiol. 2014;87:1-12.
Not in our library10.1259/bjr.20130676
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Castro J.R., Saunders W.M., Tobias C.A., Chen G.T.Y., Curtis S., Lyman J.T., Michael Collier J., Pitluck S., Woodruff K.A., Blakely E.A., et al. Treatment of cancer with heavy charged particles. Int. J. Radiat. Oncol. Biol. Phys. 1982;8:2191-2198.
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Nakano T., Suzuki Y., Ohno T., Kato S., Suzuki M., Morita S., Sato S., Oka K., Tsujii H. Carbon beam therapy overcomes the radiation resistance of uterine cervical cancer originating from hypoxia. Clin. Cancer Res. 2006;12:2185-2190.
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156.
Huart C., Chen J., Le Calvé B., Michiels C., Wéra A.-C. Could Protons and Carbon Ions Be the Silver Bullets Against Pancreatic Cancer? Int. J. Mol. Sci. 2020;21:4767.
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Koong A.C., Mehta V.K., Le Q.T., Fisher G.A., Terris D.J., Brown J.M., Bastidas A.J., Vierra M. Pancreatic tumors show high levels of hypoxia. Int. J. Radiat. Oncol. Biol. Phys. 2000;48:919-922.
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Tinganelli W., Durante M., Hirayama R., Krämer M., Maier A., Kraft-Weyrather W., Furusawa Y., Friedrich T., Scifoni E. Kill-painting of hypoxic tumours in charged particle therapy. Sci. Rep. 2015;5:17016.
Not in our library10.1038/srep17016
159.
Scifoni E., Tinganelli W., Weyrather W.K., Durante M., Maier A., Krämer M. Including oxygen enhancement ratio in ion beam treatment planning: Model implementation and experimental verification. Phys. Med. Biol. 2013;58:3871-3895.
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160.
Dokic I., Mairani A., Niklas M., Zimmermann F., Chaudhri N., Krunic D., Tessonnier T., Ferrari A., Parodi K., Jäkel O., et al. Next generation multi-scale biophysical characterization of high precision cancer particle radiotherapy using clinical proton, helium-, carbon- and oxygen ion beams. Oncotarget. 2016;7:56676-56689.
Not in our library10.18632/oncotarget.10996
161.
Kurz C., Mairani A., Parodi K. First experimental-based characterization of oxygen ion beam depth dose distributions at the Heidelberg Ion-Beam Therapy Center. Phys. Med. Biol. 2012;57:5017-5034.
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Inaniwa T., Kanematsu N., Noda K., Kamada T. Treatment planning of intensity modulated composite particle therapy with dose and linear energy transfer optimization. Phys. Med. Biol. 2017;62:5180-5197.
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163.
Toma-Dasu I., Uhrdin J., Antonovic L., Dasu A., Nuyts S., Dirix P., Haustermans K., Brahme A. Dose prescription and treatment planning based on FMISO-PET hypoxia. Acta Oncol. (Madr.). 2012;51:222-230.
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Mortensen L.S., Buus S., Nordsmark M., Bentzen L., Munk O.L., Keiding S., Overgaard J. Identifying hypoxia in human tumors: A correlation study between 18F-FMISO PET and the Eppendorf oxygen-sensitive electrode. Acta Oncol. 2010;49:934-940.
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165.
Dubois L.J., Lieuwes N.G., Janssen M.H.M., Peeters W.J.M., Windhorst A.D., Walsh J.C., Kolb H.C., Ollers M.C., Bussink J., van Dongen G.A.M.S., et al. Preclinical evaluation and validation of [18F]HX4, a promising hypoxia marker for PET imaging. Proc. Natl. Acad. Sci. USA. 2011;108:14620-14625.
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Tinganelli W., Ma N.-Y., Von Neubeck C., Maier A., Schicker C., Kraft-Weyrather W., Durante M. Influence of acute hypoxia and radiation quality on cell survival. J. Radiat. Res. 2013;54:i23-i30.
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Ma N.-Y., Tinganelli W., Maier A., Durante M., Kraft-Weyrather W. Influence of chronic hypoxia and radiation quality on cell survival. J. Radiat. Res. 2013;54:i13-i22.
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Hirayama R., Uzawa A., Takase N., Matsumoto Y., Noguchi M., Koda K., Ozaki M., Yamashita K., Li H., Kase Y., et al. Evaluation of SCCVII tumor cell survival in clamped and non-clamped solid tumors exposed to carbon-ion beams in comparison to X-rays. Mutat. Res. Toxicol. Environ. Mutagen. 2013;756:146-151.
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Fukawa T., Takematsu K., Oka K., Koike S., Ando K., Kobayashi H., Tanishita K. Differences in pO2 Peaks of a Murine Fibrosarcoma between Carbon-ion and X-ray Irradiation. J. Radiat. Res. 2004;45:303-308.
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Ando K., Koike S., Ohira C., Chen Y.J., Nojima K., Ando S., Ohbuchi T., Kobayashi N., Shimizu W., Urano M. Accelerated reoxygenation of a murine fibrosarcoma after carbon-ion radiation. Int. J. Radiat. Biol. 1999;75:505-512.
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Bendinger A.L., Seyler L., Saager M., Debus C., Peschke P., Komljenovic D., Debus J., Peter J., Floca R.O., Karger C.P., et al. Impact of Single Dose Photons and Carbon Ions on Perfusion and Vascular Permeability: A Dynamic Contrast-Enhanced MRI Pilot Study in the Anaplastic Rat Prostate Tumor R3327-AT1. Radiat. Res. 2019;193:34.
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Semenza G.L. Pharmacologic Targeting of Hypoxia-Inducible Factors. Annu. Rev. Pharmacol. Toxicol. 2019;59:379-403.
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173.
New horizons in hypoxia signaling pathways · 2017
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174.
Subtil F.S.B., Wilhelm J., Bill V., Westholt N., Rudolph S., Fischer J., Scheel S., Seay U., Fournier C., Taucher-Scholz G., et al. Carbon ion radiotherapy of human lung cancer attenuates HIF-1 signaling and acts with considerably enhanced therapeutic efficiency. FASEB J. 2014;28:1412-1421.
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Valable S., Gérault A.N., Lambert G., Leblond M.M., Anfray C., Toutain J., Bordji K., Petit E., Bernaudin M., Pérès E.A. Impact of Hypoxia on Carbon Ion Therapy in Glioblastoma Cells: Modulation by LET and Hypoxia-Dependent Genes. Cancers. 2020;12:2019.
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Wozny A.-S., Lauret A., Battiston-Montagne P., Guy J.-B., Beuve M., Cunha M., Saintigny Y., Blond E., Magne N., Lalle P., et al. Differential pattern of HIF-1α expression in HNSCC cancer stem cells after carbon ion or photon irradiation: One molecular explanation of the oxygen effect. Br. J. Cancer. 2017;116:1340-1349.
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177.
Wozny A.-S., Vares G., Alphonse G., Lauret A., Monini C., Magné N., Cuerq C., Fujimori A., Monboisse J.-C., Beuve M., et al. ROS Production and Distribution: A New Paradigm to Explain the Differential Effects of X-ray and Carbon Ion Irradiation on Cancer Stem Cell Migration and Invasion. Cancers. 2019;11:468.
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Baumann M., Krause M., Overgaard J., Debus J., Bentzen S.M., Daartz J., Richter C., Zips D., Bortfeld T. Radiation oncology in the era of precision medicine. Nat. Rev. Cancer. 2016;16:234-249.
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Kerns S.L., Chuang K.-H., Hall W., Werner Z., Chen Y., Ostrer H., West C., Rosenstein B. Radiation biology and oncology in the genomic era. Br. J. Radiol. 2018;91:20170949.
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Rosenstein B.S. Radiogenomics: Identification of Genomic Predictors for Radiation Toxicity. Semin. Radiat. Oncol. 2017;27:300-309.
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West C., Rosenstein B.S. Establishment of a Radiogenomics Consortium. Int. J. Radiat. Oncol. 2010;76:1295-1296.
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Barnett G.C., West C.M.L., Dunning A.M., Elliott R.M., Coles C.E., Pharoah P.D.P., Burnet N.G. Normal tissue reactions to radiotherapy: Towards tailoring treatment dose by genotype. Nat. Rev. Cancer. 2009;9:134-142.
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Bergom C., West C.M., Higginson D.S., Abazeed M.E., Arun B., Bentzen S.M., Bernstein J.L., Evans J.D., Gerber N.K., Kerns S.L., et al. The Implications of Genetic Testing on Radiation Therapy Decisions: A Guide for Radiation Oncologists. Int. J. Radiat. Oncol. 2019;105:698-712.
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184.
Swift M., Morrell D., Massey R.B., Chase C.L. Incidence of Cancer in 161 Families Affected by Ataxia–Telangiectasia. N. Engl. J. Med. 1991;325:1831-1836.
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185.
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Suetens A., Moreels M., Quintens R., Chiriotti S., Tabury K., Michaux A., Grégoire V., Baatout S. Carbon ion irradiation of the human prostate cancer cell line PC3: A whole genome microarray study. Int. J. Oncol. 2014;44:1056-1072.
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Luft S., Arrizabalaga O., Kulish I., Nasonova E., Durante M., Ritter S., Schroeder I.S. Ionizing Radiation Alters Human Embryonic Stem Cell Properties and Differentiation Capacity by Diminishing the Expression of Activin Receptors. Stem Cells Dev. 2017;26:341-352.
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Visvader J.E., Lindeman G.J. Cancer stem cells in solid tumours: Accumulating evidence and unresolved questions. Nat. Rev. Cancer. 2008;8:755-768.
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Najafi M., Farhood B., Mortezaee K., Kharazinejad E., Majidpoor J., Ahadi R. Hypoxia in solid tumors: A key promoter of cancer stem cell (CSC) resistance. J. Cancer Res. Clin. Oncol. 2020;146:19-31.
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Cui X., Oonishi K., Tsujii H., Yasuda T., Matsumoto Y., Furusawa Y., Akashi M., Kamada T., Okayasu R. Effects of carbon ion beam on putative colon cancer stem cells and its comparison with X-rays. Cancer Res. 2011;71:3676-3687.
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Sai S., Wakai T., Vares G., Yamada S., Kamijo T., Kamada T., Shirai T. Combination of carbon ion beam and gemcitabine causes irreparable DNA damage and death of radioresistant pancreatic cancer stem-like cells in vitro and in vivo. Oncotarget. 2015;6:5517-5535.
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Sai S., Vares G., Kim E.H., Karasawa K., Wang B., Nenoi M., Horimoto Y., Hayashi M. Carbon ion beam combined with cisplatin effectively disrupts triple negative breast cancer stem-like cells in vitro. Mol. Cancer. 2015;14:166.
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Takahashi M., Hirakawa H., Yajima H., Izumi-Nakajima N., Okayasu R., Fujimori A. Carbon ion beam is more effective to induce cell death in sphere-type A172 human glioblastoma cells compared with X-rays. Int. J. Radiat. Biol. 2014;90:1125-1132.
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Combs S.E., Zipp L., Rieken S., Habermehl D., Brons S., Winter M., Haberer T., Debus J., Weber K.-J. In vitro evaluation of photon and carbon ion radiotherapy in combination with chemotherapy in glioblastoma cells. Radiat. Oncol. 2012;7:9.
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Evolution of Cancer Pharmacological Treatments at the Turn of the Third Millennium · 2018
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Chae Y.K., Pan A.P., Davis A.A., Patel S.P., Carneiro B.A., Kurzrock R., Giles F.J. Path toward Precision Oncology: Review of Targeted Therapy Studies and Tools to Aid in Defining “Actionability” of a Molecular Lesion and Patient Management Support. Mol. Cancer Ther. 2017;16:2645-2655.
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Gatzka M. Targeted Tumor Therapy Remixed—An Update on the Use of Small-Molecule Drugs in Combination Therapies. Cancers. 2018;10:155.
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Vares G., Ahire V., Sunada S., Ho Kim E., Sai S., Chevalier F., Romeo P.-H., Yamamoto T., Nakajima T., Saintigny Y. A multimodal treatment of carbon ions irradiation, miRNA-34 and mTOR inhibitor specifically control high-grade chondrosarcoma cancer stem cells. Radiother. Oncol. 2020;150:253-261.
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Hirai T., Shirai H., Fujimori H., Okayasu R., Sasai K., Masutani M. Radiosensitization effect of poly(ADP-ribose) polymerase inhibition in cells exposed to low and high liner energy transfer radiation. Cancer Sci. 2012;103:1045-1050.
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Lesueur P., Chevalier F., El-Habr E.A., Junier M.-P., Chneiweiss H., Castera L., Müller E., Stefan D., Saintigny Y. Radiosensitization Effect of Talazoparib, a Parp Inhibitor, on Glioblastoma Stem Cells Exposed to Low and High Linear Energy Transfer Radiation. Sci. Rep. 2018;8:3664.
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Yang L., Liu Y., Sun C., Yang X., Yang Z., Ran J., Zhang Q., Zhang H., Wang X., Wang X. Inhibition of DNA-PKcs enhances radiosensitivity and increases the levels of ATM and ATR in NSCLC cells exposed to carbon ion irradiation. Oncol. Lett. 2015;10:2856-2864.
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Lee Y., Sunada S., Hirakawa H., Fujimori A., Nickoloff J.A., Okayasu R. TAS-116, a Novel Hsp90 Inhibitor, Selectively Enhances Radiosensitivity of Human Cancer Cells to X-rays and Carbon Ion Radiation. Mol. Cancer Ther. 2017;16:16-24.
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Lee Y., Li H.K., Masaoka A., Sunada S., Hirakawa H., Fujimori A., Nickoloff J.A., Okayasu R. The purine scaffold Hsp90 inhibitor PU-H71 sensitizes cancer cells to heavy ion radiation by inhibiting DNA repair by homologous recombination and non-homologous end joining. Radiother. Oncol. 2016;121:162-168.
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Konings K., Vandevoorde C., Belmans N., Vermeesen R., Baselet B., Van Walleghem M., Janssen A., Isebaert S., Baatout S., Haustermans K., et al. The Combination of Particle Irradiation With the Hedgehog Inhibitor GANT61 Differently Modulates the Radiosensitivity and Migration of Cancer Cells Compared to X-Ray Irradiation. Front. Oncol. 2019;9.
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Konings K., Belmans N., Vermeesen R., Baselet B., Lamers G., Janssen A., Isebaert S., Baatout S., Haustermans K., Moreels M. Targeting the Hedgehog pathway in combination with X-ray or carbon ion radiation decreases migration of MCF-7 breast cancer cells. Int. J. Oncol. 2019.
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Jain S., Hirst D.G., O’Sullivan J.M. Gold nanoparticles as novel agents for cancer therapy. Br. J. Radiol. 2012;85:101-113.
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Gold Nanoparticles as a Potent Radiosensitizer: A Transdisciplinary Approach from Physics to Patient · 2020
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249.
Howard D., Sebastian S., Le Q.V.-C., Thierry B., Kempson I. Chemical Mechanisms of Nanoparticle Radiosensitization and Radioprotection: A Review of Structure-Function Relationships Influencing Reactive Oxygen Species. Int. J. Mol. Sci. 2020;21:579.
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Jeremic B., Aguerri A.R., Filipovic N. Radiosensitization by gold nanoparticles. Clin. Transl. Oncol. 2013;15:593-601.
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253.
Peukert D., Kempson I., Douglass M., Bezak E. Metallic nanoparticle radiosensitisation of ion radiotherapy: A review. Phys. Med. 2018;47:121-128.
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Lacombe S., Porcel E., Scifoni E. Particle therapy and nanomedicine: State of art and research perspectives. Cancer Nanotechnol. 2017;8:9.
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Fuss M.C., Boscolo D., Durante M., Scifoni E., Krämer M. Systematic quantification of nanoscopic dose enhancement of gold nanoparticles in ion beams. Phys. Med. Biol. 2020;65:075008.
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Rudek B., McNamara A., Ramos-Méndez J., Byrne H., Kuncic Z., Schuemann J. Radio-enhancement by gold nanoparticles and their impact on water radiolysis for x-ray, proton and carbon-ion beams. Phys. Med. Biol. 2019;64:175005.
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Kirkwood J.M., Butterfield L.H., Tarhini A.A., Zarour H., Kalinski P., Ferrone S. Immunotherapy of cancer in 2012. CA Cancer J Clin. 2012;62:309-335.
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Robert C., Schachter J., Long G.V., Arance A., Grob J.J., Mortier L., Daud A., Carlino M.S., McNeil C., Lotem M., et al. Pembrolizumab versus Ipilimumab in Advanced Melanoma. N. Engl. J. Med. 2015;372:2521-2532.
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Postow M.A., Sidlow R., Hellmann M.D. Immune-Related Adverse Events Associated with Immune Checkpoint Blockade. N. Engl. J. Med. 2018;378:158-168.
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Whiteside T.L., Demaria S., Rodriguez-Ruiz M.E., Zarour H.M., Melero I. Emerging Opportunities and Challenges in Cancer Immunotherapy. Clin. Cancer Res. 2016;22:1845-1855.
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Formenti S.C., Demaria S. Systemic effects of local radiotherapy. Lancet Oncol. 2009;10:718-726.
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Ngwa W., Irabor O.C., Schoenfeld J.D., Hesser J., Demaria S., Formenti S.C. Using immunotherapy to boost the abscopal effect. Nat. Rev. Cancer. 2018;18:313-322.
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Demaria S., Golden E.B., Formenti S.C. Role of Local Radiation Therapy in Cancer Immunotherapy. JAMA Oncol. 2015;1:1325-1332.
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264.
Formenti S.C., Demaria S. Combining radiotherapy and cancer immunotherapy: A paradigm shift. J. Natl. Cancer Inst. 2013;105:256-265.
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Durante M., Reppingen N., Held K.D. Immunologically augmented cancer treatment using modern radiotherapy. Trends Mol. Med. 2013;19:565-582.
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Van Limbergen E.J., De Ruysscher D.K., Olivo Pimentel V., Marcus D., Berbee M., Hoeben A., Rekers N., Theys J., Yaromina A., Dubois L.J., et al. Combining radiotherapy with immunotherapy: The past, the present and the future. Br. J. Radiol. 2017;90:20170157.
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Herrera F.G., Bourhis J., Coukos G. Radiotherapy combination opportunities leveraging immunity for the next oncology practice. CA Cancer J. Clin. 2017;67:65-85.
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Zhao X., Shao C. Radiotherapy-Mediated Immunomodulation and Anti-Tumor Abscopal Effect Combining Immune Checkpoint Blockade. Cancers. 2020;12:2762.
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Lubas M.J., Kumar S.S. The Combined Use of SBRT and Immunotherapy—a Literature Review. Curr. Oncol. Rep. 2020;22:117.
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Victor C.T.-S., Rech A.J., Maity A., Rengan R., Pauken K.E., Stelekati E., Benci J.L., Xu B., Dada H., Odorizzi P.M., et al. Radiation and dual checkpoint blockade activate non-redundant immune mechanisms in cancer. Nature. 2015;520:373-377.
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Postow M.A., Callahan M.K., Barker C.A., Yamada Y., Yuan J., Kitano S., Mu Z., Rasalan T., Adamow M., Ritter E., et al. Immunologic correlates of the abscopal effect in a patient with melanoma. N. Engl. J. Med. 2012;366:925-931.
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Hiniker S.M., Chen D.S., Knox S.J. Abscopal Effect in a Patient with Melanoma. N. Engl. J. Med. 2012;366:2035-2036.
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Radiation-Induced Chromosomal Aberrations and Immunotherapy: Micronuclei, Cytosolic DNA, and Interferon-Production Pathway · 2018
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DNA double-strand break repair pathway regulates PD-L1 expression in cancer cells · 2017
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Space Radiation: The Number One Risk to Astronaut Health beyond Low Earth Orbit · 2014
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Role of Mitochondria in Radiation Responses: Epigenetic, Metabolic, and Signaling Impacts · 2021
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