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Translational Cancer Mechanisms and Therapy

Hypofractionated FLASH-RT as an Effective Treatment against Glioblastoma that Reduces Neurocognitive Side Effects in Mice

Pierre Montay-Gruel, Munjal M. Acharya, Patrik Gonçalves Jorge, Benoît Petit, Ioannis G. Petridis, Philippe Fuchs, Ron Leavitt, Kristoffer Petersson, Maude Gondré, Jonathan Ollivier, Raphael Moeckli, François Bochud, Claude Bailat, Jean Bourhis, Jean-François Germond, Charles L. Limoli and Marie-Catherine Vozenin
Pierre Montay-Gruel
1Laboratory of Radiation Oncology/DO/Radio-Oncology/CHUV, Lausanne University Hospital and University of Lausanne, Switzerland.
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  • ORCID record for Pierre Montay-Gruel
Munjal M. Acharya
2Department of Radiation Oncology, University of California, Irvine, California.
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  • ORCID record for Munjal M. Acharya
Patrik Gonçalves Jorge
1Laboratory of Radiation Oncology/DO/Radio-Oncology/CHUV, Lausanne University Hospital and University of Lausanne, Switzerland.
3Institute of Radiation Physics/CHUV, Lausanne University Hospital, Switzerland.
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Benoît Petit
1Laboratory of Radiation Oncology/DO/Radio-Oncology/CHUV, Lausanne University Hospital and University of Lausanne, Switzerland.
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Ioannis G. Petridis
1Laboratory of Radiation Oncology/DO/Radio-Oncology/CHUV, Lausanne University Hospital and University of Lausanne, Switzerland.
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Philippe Fuchs
1Laboratory of Radiation Oncology/DO/Radio-Oncology/CHUV, Lausanne University Hospital and University of Lausanne, Switzerland.
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Ron Leavitt
1Laboratory of Radiation Oncology/DO/Radio-Oncology/CHUV, Lausanne University Hospital and University of Lausanne, Switzerland.
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Kristoffer Petersson
1Laboratory of Radiation Oncology/DO/Radio-Oncology/CHUV, Lausanne University Hospital and University of Lausanne, Switzerland.
3Institute of Radiation Physics/CHUV, Lausanne University Hospital, Switzerland.
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Maude Gondré
1Laboratory of Radiation Oncology/DO/Radio-Oncology/CHUV, Lausanne University Hospital and University of Lausanne, Switzerland.
3Institute of Radiation Physics/CHUV, Lausanne University Hospital, Switzerland.
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Jonathan Ollivier
1Laboratory of Radiation Oncology/DO/Radio-Oncology/CHUV, Lausanne University Hospital and University of Lausanne, Switzerland.
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Raphael Moeckli
3Institute of Radiation Physics/CHUV, Lausanne University Hospital, Switzerland.
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François Bochud
3Institute of Radiation Physics/CHUV, Lausanne University Hospital, Switzerland.
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Claude Bailat
3Institute of Radiation Physics/CHUV, Lausanne University Hospital, Switzerland.
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Jean Bourhis
1Laboratory of Radiation Oncology/DO/Radio-Oncology/CHUV, Lausanne University Hospital and University of Lausanne, Switzerland.
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Jean-François Germond
3Institute of Radiation Physics/CHUV, Lausanne University Hospital, Switzerland.
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Charles L. Limoli
2Department of Radiation Oncology, University of California, Irvine, California.
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Marie-Catherine Vozenin
1Laboratory of Radiation Oncology/DO/Radio-Oncology/CHUV, Lausanne University Hospital and University of Lausanne, Switzerland.
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  • For correspondence: marie-catherine.vozenin@chuv.ch
DOI: 10.1158/1078-0432.CCR-20-0894 Published February 2021
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Abstract

Purpose: Recent data have shown that single-fraction irradiation delivered to the whole brain in less than tenths of a second using FLASH radiotherapy (FLASH-RT), does not elicit neurocognitive deficits in mice. This observation has important clinical implications for the management of invasive and treatment-resistant brain tumors that involves relatively large irradiation volumes with high cytotoxic doses.

Experimental Design: Therefore, we aimed at simultaneously investigating the antitumor efficacy and neuroprotective benefits of FLASH-RT 1-month after exposure, using a well-characterized murine orthotopic glioblastoma model. As fractionated regimens of radiotherapy are the standard of care for glioblastoma treatment, we incorporated dose fractionation to simultaneously validate the neuroprotective effects and optimized tumor treatments with FLASH-RT.

Results: The capability of FLASH-RT to minimize the induction of radiation-induced brain toxicities has been attributed to the reduction of reactive oxygen species, casting some concern that this might translate to a possible loss of antitumor efficacy. Our study shows that FLASH and CONV-RT are isoefficient in delaying glioblastoma growth for all tested regimens. Furthermore, only FLASH-RT was found to significantly spare radiation-induced cognitive deficits in learning and memory in tumor-bearing animals after the delivery of large neurotoxic single dose or hypofractionated regimens.

Conclusions: The present results show that FLASH-RT delivered with hypofractionated regimens is able to spare the normal brain from radiation-induced toxicities without compromising tumor cure. This exciting capability provides an initial framework for future clinical applications of FLASH-RT.

See related commentary by Huang and Mendonca, p. 662

Footnotes

  • Note: Supplementary data for this article are available at Clinical Cancer Research Online (http://clincancerres.aacrjournals.org/).

  • Clin Cancer Res 2021;27:775–84

  • Received March 18, 2020.
  • Revision received September 3, 2020.
  • Accepted October 12, 2020.
  • Published first October 15, 2020.
  • ©2020 American Association for Cancer Research.
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Clinical Cancer Research: 27 (3)
February 2021
Volume 27, Issue 3
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Hypofractionated FLASH-RT as an Effective Treatment against Glioblastoma that Reduces Neurocognitive Side Effects in Mice
Pierre Montay-Gruel, Munjal M. Acharya, Patrik Gonçalves Jorge, Benoît Petit, Ioannis G. Petridis, Philippe Fuchs, Ron Leavitt, Kristoffer Petersson, Maude Gondré, Jonathan Ollivier, Raphael Moeckli, François Bochud, Claude Bailat, Jean Bourhis, Jean-François Germond, Charles L. Limoli and Marie-Catherine Vozenin
Clin Cancer Res February 1 2021 (27) (3) 775-784; DOI: 10.1158/1078-0432.CCR-20-0894

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Hypofractionated FLASH-RT as an Effective Treatment against Glioblastoma that Reduces Neurocognitive Side Effects in Mice
Pierre Montay-Gruel, Munjal M. Acharya, Patrik Gonçalves Jorge, Benoît Petit, Ioannis G. Petridis, Philippe Fuchs, Ron Leavitt, Kristoffer Petersson, Maude Gondré, Jonathan Ollivier, Raphael Moeckli, François Bochud, Claude Bailat, Jean Bourhis, Jean-François Germond, Charles L. Limoli and Marie-Catherine Vozenin
Clin Cancer Res February 1 2021 (27) (3) 775-784; DOI: 10.1158/1078-0432.CCR-20-0894
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