Review
. 2017 Mar; 14(8):483-495.
doi: 10.1038/nrclinonc.2017.30.

Charged-particle therapy in cancer: clinical uses and future perspectives

Marco Durante 1 Roberto Orecchia 2 Jay S Loeffler 3 
Affiliations
  • PMID: 28290489
  •     121 References
  •     73 citations

Abstract

Radiotherapy with high-energy charged particles has become an attractive therapeutic option for patients with several tumour types because this approach better spares healthy tissue from radiation than conventional photon therapy. The cost associated with the delivery of charged particles, however, is higher than that of even the most elaborate photon-delivery technologies. Reliable evidence of the relative cost-effectiveness of both modalities can only come from the results of randomized clinical trials. Thus, the hurdles that currently limit direct comparisons of these two approaches in clinical trials, especially those related to insurance coverage, should be removed. Herein, we review several randomized trials of charged-particle therapies that are ongoing, with results that will enable selective delivery to patients who are most likely to benefit from them. We also discuss aspects related to radiobiology, including the immune response and hypoxia, which will need to be taken into consideration in future randomized trials to fully exploit the potential of charged particles.

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Juliette Thariat, Jean-Michel Hannoun-Levi, +2 authors, Jean-Pierre Gérard.
Nat Rev Clin Oncol, 2012 Nov 28; 10(1). PMID: 23183635
Review.
Chromosome inversions in lymphocytes of prostate cancer patients treated with X-rays and carbon ions.
Diana Pignalosa, Ryonfa Lee, +5 authors, Marco Durante.
Radiother Oncol, 2013 Nov 05; 109(2). PMID: 24183064
Risk of ischemic heart disease in women after radiotherapy for breast cancer.
Sarah C Darby, Marianne Ewertz, +13 authors, Per Hall.
N Engl J Med, 2013 Mar 15; 368(11). PMID: 23484825
Highly Cited.
Radical prostatectomy versus high-dose irradiation in localized/locally advanced prostate cancer: A Swedish multicenter randomized trial with patient-reported outcomes.
Bo Lennernäs, Khairul Majumder, +7 authors, Sten Nilsson.
Acta Oncol, 2014 Nov 05; 54(6). PMID: 25362844
Stereotactic Body Radiation Therapy for Early-Stage Lung Cancer.
Genevieve Maquilan, Robert Timmerman.
Cancer J, 2016 Jul 22; 22(4). PMID: 27441747
Review.
Defining normoxia, physoxia and hypoxia in tumours-implications for treatment response.
S R McKeown.
Br J Radiol, 2014 Mar 05; 87(1035). PMID: 24588669    Free PMC article.
Highly Cited. Review.
A 4D-optimization concept for scanned ion beam therapy.
Christian Graeff, Robert Lüchtenborg, +2 authors, Christoph Bert.
Radiother Oncol, 2013 Nov 05; 109(3). PMID: 24183865
The 150 most important questions in cancer research and clinical oncology series: questions 67-75 : Edited by Chinese Journal of Cancer.
Chinese Journal of Cancer.
Chin J Cancer, 2017 Nov 03; 36(1). PMID: 29092716    Free PMC article.
Radiation therapy-induced metastasis: radiobiology and clinical implications.
Benjamin J Blyth, Aidan J Cole, Michael P MacManus, Olga A Martin.
Clin Exp Metastasis, 2017 Nov 22; 35(4). PMID: 29159430
Review.
Particle therapy and nanomedicine: state of art and research perspectives.
Sandrine Lacombe, Erika Porcel, Emanuele Scifoni.
Cancer Nanotechnol, 2017 Dec 08; 8(1). PMID: 29213338    Free PMC article.
Review.
Recent advances in radiation oncology.
Cristina Garibaldi, Barbara Alicja Jereczek-Fossa, +8 authors, Rosalinda Ricotti.
Ecancermedicalscience, 2017 Dec 12; 11. PMID: 29225692    Free PMC article.
Review.
Editorial: Charged Particles in Oncology.
Marco Durante, Francis A Cucinotta, Jay S Loeffler.
Front Oncol, 2017 Dec 26; 7. PMID: 29276698    Free PMC article.
3D-structured illumination microscopy reveals clustered DNA double-strand break formation in widespread γH2AX foci after high LET heavy-ion particle radiation.
Yoshihiko Hagiwara, Atsuko Niimi, +8 authors, Atsushi Shibata.
Oncotarget, 2018 Jan 10; 8(65). PMID: 29312614    Free PMC article.
Effects of crystallographic and geometric orientation on ion beam sputtering of gold nanorods.
J A Hinks, F Hibberd, +7 authors, K Nordlund.
Sci Rep, 2018 Jan 13; 8(1). PMID: 29323118    Free PMC article.
New insights in the relative radiobiological effectiveness of proton irradiation.
K Ilicic, S E Combs, T E Schmid.
Radiat Oncol, 2018 Jan 18; 13(1). PMID: 29338744    Free PMC article.
Review.
Radiation-Induced Cardiovascular Disease: Mechanisms and Importance of Linear Energy Transfer.
Christopher B Sylvester, Jun-Ichi Abe, Zarana S Patel, K Jane Grande-Allen.
Front Cardiovasc Med, 2018 Feb 16; 5. PMID: 29445728    Free PMC article.
Review.
Evolution of Carbon Ion Radiotherapy at the National Institute of Radiological Sciences in Japan.
Osama Mohamad, Hirokazu Makishima, Tadashi Kamada.
Cancers (Basel), 2018 Mar 07; 10(3). PMID: 29509684    Free PMC article.
Review.
Assessing the uncertainty in a normal tissue complication probability difference (∆NTCP): radiation-induced liver disease (RILD) in liver tumour patients treated with proton vs X-ray therapy.
Keiji Kobashi, Anussara Prayongrat, +6 authors, Hiroki Shirato.
J Radiat Res, 2018 Mar 15; 59(suppl_1). PMID: 29538699    Free PMC article.
Do protons and X-rays induce cell-killing in human peripheral blood lymphocytes by different mechanisms?
J Miszczyk, K Rawojć, +5 authors, A Gałaś.
Clin Transl Radiat Oncol, 2018 Mar 30; 9. PMID: 29594247    Free PMC article.
Case-report: Metastases in a low-stage middle-graded HCC in cleared HCV infection, non-cirrhotic liver: Surgical therapy.
Stefania Brozzetti, Simone Bini, +4 authors, Giorgio De Toma.
Int J Surg Case Rep, 2018 Apr 29; 47. PMID: 29704738    Free PMC article.
Radiation-Induced Chromosomal Aberrations and Immunotherapy: Micronuclei, Cytosolic DNA, and Interferon-Production Pathway.
Marco Durante, Silvia C Formenti.
Front Oncol, 2018 Jun 19; 8. PMID: 29911071    Free PMC article.
Review.
Investigating Dependencies of Relative Biological Effectiveness for Proton Therapy in Cancer Cells.
Michelle E Howard, Chris Beltran, +3 authors, Michael G Herman.
Int J Part Ther, 2018 Aug 31; 4(3). PMID: 30159358    Free PMC article.
Mutational analysis of uterine cervical cancer that survived multiple rounds of radiotherapy.
Endang Nuryadi, Yasushi Sasaki, +20 authors, Takashi Nakano.
Oncotarget, 2018 Sep 18; 9(66). PMID: 30220971    Free PMC article.
Phase I Study of Carbon Ion Radiotherapy and Image-Guided Brachytherapy for Locally Advanced Cervical Cancer.
Tatsuya Ohno, Shin-Ei Noda, +10 authors, Working Group for Gynecologic Cancer.
Cancers (Basel), 2018 Sep 21; 10(9). PMID: 30231543    Free PMC article.
Radiotherapy improves the survival of patients with stage IV NSCLC: A propensity score matched analysis of the SEER database.
Rui Zhang, Ping Li, +5 authors, Zhenming Fu.
Cancer Med, 2018 Sep 22; 7(10). PMID: 30239162    Free PMC article.
The Relative Biological Effect of Spread-Out Bragg Peak Protons in Sensitive and Resistant Tumor Cells.
Yu-Fen Lin, Benjamin P Chen, +6 authors, Leo E Gerweck.
Int J Part Ther, 2018 Oct 05; 4(3). PMID: 30283809    Free PMC article.
Opportunistic dose amplification for proton and carbon ion therapy via capture of internally generated thermal neutrons.
Mitra Safavi-Naeini, Andrew Chacon, +4 authors, Anatoly Rosenfeld.
Sci Rep, 2018 Nov 06; 8(1). PMID: 30390002    Free PMC article.
Radiogenomic Predictors of Adverse Effects following Charged Particle Therapy.
Lindsay M Morton, Luisel Ricks-Santi, Catharine M L West, Barry S Rosenstein.
Int J Part Ther, 2018 Dec 07; 5(1). PMID: 30505881    Free PMC article.
FGFR Signaling as a Candidate Therapeutic Target for Cancers Resistant to Carbon Ion Radiotherapy.
Narisa Dewi Maulany Darwis, Ankita Nachankar, +21 authors, Takashi Nakano.
Int J Mol Sci, 2019 Sep 22; 20(18). PMID: 31540114    Free PMC article.
Validation of the RayStation Monte Carlo dose calculation algorithm using realistic animal tissue phantoms.
Andries N Schreuder, Daniel S Bridges, +4 authors, John B Wilkinson.
J Appl Clin Med Phys, 2019 Sep 22; 20(10). PMID: 31541536    Free PMC article.
Three discipline collaborative radiation therapy (3DCRT) special debate: The United States needs at least one carbon ion facility.
Eleanor A Blakely, Bruce Faddegon, +5 authors, Jay Burmeister.
J Appl Clin Med Phys, 2019 Oct 02; 20(11). PMID: 31573146    Free PMC article.
Combining Heavy-Ion Therapy with Immunotherapy: An Update on Recent Developments.
Alexander Helm, Daniel K Ebner, +6 authors, Takashi Shimokawa.
Int J Part Ther, 2018 Jul 01; 5(1). PMID: 31773022    Free PMC article.
Review.
Strategies to Enhance Radiosensitivity to Heavy Ion Radiation Therapy.
Younghyun Lee, Ryuichi Okayasu.
Int J Part Ther, 2018 Jul 01; 5(1). PMID: 31773023    Free PMC article.
Review.
Combined Treatment Modalities for High-Energy Proton Irradiation: Exploiting Specific DNA Repair Dependencies.
Simon Deycmar, Martin Pruschy.
Int J Part Ther, 2018 Jul 01; 5(1). PMID: 31773025    Free PMC article.
Review.
Moderately hypofractionated carbon ion radiotherapy for prostate cancer; a prospective observational study "GUNMA0702".
Hidemasa Kawamura, Nobuteru Kubo, +9 authors, Group for Genitourinary Tumors at Gunma University Heavy Ion Medical Center.
BMC Cancer, 2020 Feb 01; 20(1). PMID: 32000716    Free PMC article.
Carbon Ion Therapy: A Modern Review of an Emerging Technology.
Timothy D Malouff, Anita Mahajan, +3 authors, Daniel Michael Trifiletti.
Front Oncol, 2020 Mar 03; 10. PMID: 32117737    Free PMC article.
Review.
Clinical trials involving carbon-ion radiation therapy and the path forward.
Ann A Lazar, Reinhard Schulte, +2 authors, Mack Roach.
Cancer, 2018 Oct 12; 124(23). PMID: 30307603    Free PMC article.
Review.
Proton beam therapy in Europe: more centres need more research.
Marco Durante.
Br J Cancer, 2018 Dec 12; 120(8). PMID: 30531831    Free PMC article.
Comparison of the effects of photon, proton and carbon-ion radiation on the ecto-calreticulin exposure in various tumor cell lines.
Yangle Huang, Yuanli Dong, +3 authors, Jiade Jay Lu.
Ann Transl Med, 2019 Dec 07; 7(20). PMID: 31807524    Free PMC article.
Master Protocol Trial Design for Efficient and Rational Evaluation of Novel Therapeutic Oncology Devices.
Danielle S Bitterman, Daniel N Cagney, +3 authors, Raymond H Mak.
J Natl Cancer Inst, 2019 Sep 11; 112(3). PMID: 31504680    Free PMC article.
Review.
Harnessing radiation to improve immunotherapy: better with particles?
Marco Durante, Silvia Formenti.
Br J Radiol, 2019 Jul 19; 93(1107). PMID: 31317768    Free PMC article.
Proton RBE dependence on dose in the setting of hypofractionation.
Thomas Friedrich.
Br J Radiol, 2019 Aug 23; 93(1107). PMID: 31437004    Free PMC article.
Review.
Long-time clinical experience in patient setup for several particle therapy clinical indications: management of patient positioning and evaluation of setup reproducibility and stability.
Rosalinda Ricotti, Andrea Pella, +7 authors, Guido Baroni.
Br J Radiol, 2019 Nov 07; 93(1107). PMID: 31687833    Free PMC article.
The relative biological effectiveness of proton irradiation in dependence of DNA damage repair.
Simon Deycmar, Erica Faccin, +8 authors, Martin Pruschy.
Br J Radiol, 2019 Nov 07; 93(1107). PMID: 31687835    Free PMC article.
Review.
Radiation-Induced DNA Damage Cooperates with Heterozygosity of TP53 and PTEN to Generate High-Grade Gliomas.
Pavlina K Todorova, Eliot Fletcher-Sananikone, +12 authors, Sandeep Burma.
Cancer Res, 2019 May 16; 79(14). PMID: 31088835    Free PMC article.
Medical Gas Plasma Jet Technology Targets Murine Melanoma in an Immunogenic Fashion.
Sander Bekeschus, Ramona Clemen, +3 authors, Anke Schmidt.
Adv Sci (Weinh), 2020 May 23; 7(10). PMID: 32440479    Free PMC article.
Specificity of end resection pathways for double-strand break regions containing ribonucleotides and base lesions.
James M Daley, Nozomi Tomimatsu, +10 authors, Patrick Sung.
Nat Commun, 2020 Jun 20; 11(1). PMID: 32555206    Free PMC article.
Proton Therapy for Locally Advanced Oropharyngeal Cancer: Initial Clinical Experience at the University of Washington.
Saif Aljabab, Andrew Liu, +3 authors, Upendra Parvathaneni.
Int J Part Ther, 2020 Jun 26; 6(3). PMID: 32582809    Free PMC article.
Technology-driven research for radiotherapy innovation.
Claudio Fiorino, Matthias Guckemberger, +2 authors, Ben Heijmen.
Mol Oncol, 2020 Mar 04; 14(7). PMID: 32124546    Free PMC article.
Review.
Novel strategies using modern radiotherapy to improve pancreatic cancer outcomes: toward a new standard?
Christelle Bouchart, Julie Navez, +4 authors, Jean-Luc Van Laethem.
Ther Adv Med Oncol, 2020 Jul 21; 12. PMID: 32684987    Free PMC article.
Review.
Dosimetric evaluation of MR-derived synthetic-CTs for MR-only proton treatment planning.
David Aramburu Núñez, Sandra Fontenla, +5 authors, Neelam Tyagi.
Med Dosim, 2020 Feb 25; 45(3). PMID: 32089396    Free PMC article.
The societal impact of ion beam therapy.
Thomas R Bortfeld, Matthew Fernandez de Viana, Susu Yan.
Z Med Phys, 2020 Jul 19; 31(2). PMID: 32680688    Free PMC article.
Small-molecule drug repurposing to target DNA damage repair and response pathways.
Jacqueline A Brinkman, Yue Liu, Stephen J Kron.
Semin Cancer Biol, 2020 Mar 03; 68. PMID: 32113999    Free PMC article.
Review.
The Determinant of DNA Repair Pathway Choices in Ionising Radiation-Induced DNA Double-Strand Breaks.
Lei Zhao, Chengyu Bao, +5 authors, Yeqing Sun.
Biomed Res Int, 2020 Sep 11; 2020. PMID: 32908893    Free PMC article.
Review.
Applying Precision Oncology Principles in Radiation Oncology.
Sophia C Kamran, Kent W Mouw.
JCO Precis Oncol, 2018 May 14; 2. PMID: 32914000    Free PMC article.
Review.
Radiotherapy improves the survival of patients with extensive-disease small-cell lung cancer: a propensity score matched analysis of Surveillance, Epidemiology, and End Results database.
Rui Zhang, Ping Li, +5 authors, Zhenming Fu.
Cancer Manag Res, 2018 Dec 18; 10. PMID: 30555258    Free PMC article.
Gene Expression Studies for the Development of Particle Therapy.
Sally A Amundson.
Int J Part Ther, 2018 Dec 18; 5(1). PMID: 30555854    Free PMC article.
Comparison of transcriptional profiles in human lymphocyte cells irradiated with 12C ion beams at 0-2.0 Gy.
Ruifeng Zhang, Xuhong Dang, +4 authors, Yahui Zuo.
Cancer Manag Res, 2019 Apr 10; 11. PMID: 30962723    Free PMC article.
The 6th R of Radiobiology: Reactivation of Anti-Tumor Immune Response.
Jihane Boustani, Mathieu Grapin, +2 authors, Céline Mirjolet.
Cancers (Basel), 2019 Jun 23; 11(6). PMID: 31226866    Free PMC article.
Review.
Systematic review of methodology used in clinical studies evaluating the benefits of proton beam therapy.
Mercy Ofuya, Lucy McParland, +3 authors, Emma Hall.
Clin Transl Radiat Oncol, 2019 Aug 03; 19. PMID: 31372521    Free PMC article.
Particle Beam Radiation Therapy for Skull Base Sarcomas.
Jing Yang, Weixu Hu, +7 authors, Jiade J Lu.
Front Oncol, 2020 Oct 13; 10. PMID: 33042790    Free PMC article.
Heat-killed Salmonella Typhimurium protects mice against carbon ion radiation.
Zebin Liao, Zhe Liu, +8 authors, Jianming Cai.
J Int Med Res, 2020 Oct 07; 48(10). PMID: 33021413    Free PMC article.
Particle Beam Radiation Therapy for Adenoid Cystic Carcinoma of the Nasal Cavity and Paranasal Sinuses.
Weixu Hu, Jiyi Hu, +5 authors, Jiade J Lu.
Front Oncol, 2020 Oct 27; 10. PMID: 33102230    Free PMC article.
Radioactive Beams in Particle Therapy: Past, Present, and Future.
Marco Durante, Katia Parodi.
Front Phys, 2020 Nov 24; 8. PMID: 33224941    Free PMC article.
Inter-fractional monitoring of [Formula: see text]C ions treatments: results from a clinical trial at the CNAO facility.
M Fischetti, G Baroni, +38 authors, A Sarti.
Sci Rep, 2020 Nov 28; 10(1). PMID: 33244102    Free PMC article.
Recruitment of 53BP1 Proteins for DNA Repair and Persistence of Repair Clusters Differ for Cell Types as Detected by Single Molecule Localization Microscopy.
Elizaveta Bobkova, Daniel Depes, +16 authors, Martin Falk.
Int J Mol Sci, 2018 Nov 25; 19(12). PMID: 30469529    Free PMC article.
Clustered DNA double-strand break formation and the repair pathway following heavy-ion irradiation.
Yoshihiko Hagiwara, Takahiro Oike, +6 authors, Atsushi Shibata.
J Radiat Res, 2018 Nov 27; 60(1). PMID: 30476166    Free PMC article.
Review.
Carbon irradiation overcomes glioma radioresistance by eradicating stem cells and forming an antiangiogenic and immunopermissive niche.
Sara Chiblak, Zili Tang, +17 authors, Amir Abdollahi.
JCI Insight, 2019 Jan 25; 4(2). PMID: 30674721    Free PMC article.
Highly Cited.
Challenges and Contradictions of Metal Nano-Particle Applications for Radio-Sensitivity Enhancement in Cancer Therapy.
Eva Pagáčová, Lenka Štefančíková, +13 authors, Martin Falk.
Int J Mol Sci, 2019 Feb 02; 20(3). PMID: 30704035    Free PMC article.
Comparison of Proton and Photon Beam Irradiation in Radiation-Induced Intestinal Injury Using a Mouse Model.
Changhoon Choi, Chansu Lee, +3 authors, Hee Chul Park.
Int J Mol Sci, 2019 Apr 20; 20(8). PMID: 30999572    Free PMC article.
Preoperative chemotherapy and carbon ions therapy for treatment of resectable and borderline resectable pancreatic adenocarcinoma: a prospective, phase II, multicentre, single-arm study.
Viviana Vitolo, Lorenzo Cobianchi, +11 authors, Francesca Valvo.
BMC Cancer, 2019 Sep 16; 19(1). PMID: 31521134    Free PMC article.
Clinical outcomes of carbon-ion radiotherapy for patients with locoregionally recurrent nasopharyngeal carcinoma.
Jiyi Hu, Qingting Huang, +7 authors, Jiade J Lu.
Cancer, 2020 Sep 16; 126(23). PMID: 32931035    Free PMC article.
The relative biological effectiveness of carbon ion radiation therapy for early stage lung cancer.
Jeho Jeong, Vicki T Taasti, Andrew Jackson, Joseph O Deasy.
Radiother Oncol, 2020 Sep 26; 153. PMID: 32976878    Free PMC article.
Comparison of biophysical models with experimental data for three cell lines in response to irradiation with monoenergetic ions.
Caterina Monini, Gersende Alphonse, +2 authors, Michaël Beuve.
Phys Imaging Radiat Oncol, 2019 Nov 20; 12. PMID: 33458290    Free PMC article.
Radiomics and Dosiomics for Predicting Local Control after Carbon-Ion Radiotherapy in Skull-Base Chordoma.
Giulia Buizza, Chiara Paganelli, +8 authors, Guido Baroni.
Cancers (Basel), 2021 Jan 23; 13(2). PMID: 33477723    Free PMC article.
Overlooked potential of positrons in cancer therapy.
Takanori Hioki, Yaser H Gholami, +6 authors, Dale L Bailey.
Sci Rep, 2021 Jan 30; 11(1). PMID: 33510222    Free PMC article.
Scarred Lung. An Update on Radiation-Induced Pulmonary Fibrosis.
Natalia Jarzebska, Ekaterina S Karetnikova, +3 authors, Peter M Spieth.
Front Med (Lausanne), 2021 Feb 02; 7. PMID: 33521012    Free PMC article.
Review.
Radiation-induced kidney toxicity: molecular and cellular pathogenesis.
Richard Klaus, Maximilian Niyazi, Bärbel Lange-Sperandio.
Radiat Oncol, 2021 Feb 27; 16(1). PMID: 33632272    Free PMC article.
Review.
Investigation of DNA Damage and Cell-Cycle Distribution in Human Peripheral Blood Lymphocytes under Exposure to High Doses of Proton Radiotherapy.
Justyna Miszczyk.
Biology (Basel), 2021 Feb 07; 10(2). PMID: 33546318    Free PMC article.
Downregulation of Mcl-1 by Panobinostat Potentiates Proton Beam Therapy in Hepatocellular Carcinoma Cells.
Changhoon Choi, Ga Haeng Lee, +3 authors, Hee Chul Park.
Cells, 2021 Apr 04; 10(3). PMID: 33806487    Free PMC article.