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Radiation therapy combined with intracerebral convection-enhanced delivery of cisplatin or carboplatin for treatment of the F98 rat glioma

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Abstract

Background

The purpose of this review is to summarize our own experimental studies carried out over a 13-year period of time using the F98 rat glioma as model for high grade gliomas. We evaluated a binary chemo-radiotherapeutic modality that combines either cisplatin (CDDP) or carboplatin, administered intracerebrally (i.c.) by means of convection-enhanced delivery (CED) or osmotic pumps, in combination with either synchrotron or conventional X-irradiation.

Methods

F98 glioma cells were implanted stereotactically into the brains of syngeneic Fischer rats. Approximately 14 days later, either CDDP or carboplatin was administered i.c. by CED, followed 24 h later by radiotherapy using either a synchrotron or, subsequently, megavoltage linear accelerators (LINAC).

Results

CDDP was administered at a dose of 3 µg in 5 µL, followed 24 h later with an irradiation dose of 15 Gy or carboplatin at a dose of 20 µg in 10 µL, followed 24 h later with 3 fractions of 8 Gy each, at the source at the European Synchrotron Radiation Facility (ESRF). This resulted in a median survival time (MeST) > 180 days with 33% long term survivors (LTS) for CDDP and a MeST > 60 days with 8 to 22% LTS, for carboplatin. Subsequently it became apparent that comparable survival data could be obtained with megavoltage X-irradiation using a LINAC source. The best survival data were obtained with a dose of 72 µg of carboplatin administered by means of Alzet® osmotic pumps over 7 days. This resulted in a MeST of > 180 days, with 55% LTS. Histopathologic examination of all the brains of the surviving rats revealed no residual tumor cells or evidence of significant radiation related effects.

Conclusions

The results obtained using this combination therapy has, to the best of our knowledge, yielded the most promising survival data ever reported using the F98 glioma model.

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Abbreviations

AZQ:

Aziridinyl-benzoquinone

BBB:

Blood–brain barrier

BBB-D:

Blood–brain barrier disruption

BCNU:

1,3-Bis (2-chloroethyl)-1-nitrosourea

C225:

Cetuximab

CED:

Convection-enhanced delivery

CDDP:

Cisplatin

CI:

Combination index

D:

Dexamethasone

DMF:

Dexamethasone, mannitol, furosemide

DRI:

Dose reduction index

DSBs:

DNA double strand breaks

ESRF:

European synchrotron radiation facility

F98EGFR :

F98 glioma cells transfected with the human gene encoding EGFR

F:

Furosemide

i.a.:

Intra-arterially

i.c.:

Intra-cerebrally

i.t.:

Intra-tumoral

i.v.:

Intra-venous

ICP-OES:

Inductively coupled plasma-optical emission spectroscopy

%ILS:

Percent increase in life span

LET:

Linear energy transfer

LINAC:

Linear accelerator

LTS:

Long term survivors

M:

Mannitol

MeST:

Median survival time

MRI:

Magnetic resonance imaging

PAMAM:

Polyamidoamine

PEP382:

13 Mer B-cell epitope

PEP455:

16 Mer HER-1 epitope

SF:

Surviving fraction

SSRT:

Stereotactic synchrotron radiotherapy

Vd :

Volume of distribution

XRT:

Conventional radiotherapy

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Acknowledgements

We thank Michael Weldon, Nilendu Gupta, and John C. Grecula for their help in carrying out radiation studies for the Barth Laboratory, W. Hans Meisen, Balveen Kaur, Pravin Kaumaya and Robert Lee for their assistance in carrying out studies relating to molecular targeting, Gong Wu for preparation of bioconjugates and Delisa Watkins and David Carpenter for their assistance in the preparation of this manuscript. We thank the ESRF for their technical support and for providing beam time and special thanks to Thierry Brochard, Christian Nemoz and Dominique Dallery. Finally, we thank Marie-Claude Biston, Jean-François Adam, Anne-Marie Charvet, Caroline Boudou and François Estève, for their help in carrying out radiation studies in Grenoble.

Funding

Support for studies, carried out by Barth and his co-workers, has been provided by the Musella Foundation, Voices against Brain Cancer, The Ohio State University Department of Pathology and the Kevin J. Mullin Memorial Fund for Brain Tumor Research. Those carried out by Elleaume and her research team were supported by the University Grenoble Alpes, INSERM, the Auvergne Rhône Alpes region and the Labex Primes (ANR-11-LABX-0063).

Author information

Author notes

  1. Jacques Balosso

    Present address: Centre de lutte contre le Cancer F. Baclesse, 3 avenue du général Harris, 14000, Caen, France

  2. Weilian Yang

    Present address: Department of Neurosurgery, Suzhou Medical College, Suzhou, China

  3. Tianyao Huo

    Present address: Department of Health Outcomes and Policy, College of Medicine, University of Florida, Gainesville, FL, 32610, USA

  4. Robin Nakkula

    Present address: Research Institute, Nationwide Children’s Hospital, Columbus, OH, 43205, USA

  5. Hélène Elleaume and Rolf F. Barth have contributed equally to this work.

Authors and Affiliations

  1. INSERM UA07 Team STROBE, ESRF, 71 Avenue des Martyrs, 38000, Grenoble, France

    Hélène Elleaume, Julia Rousseau, Laure Bobyk & Jacques Balosso

  2. Department of Pathology, The Ohio State University, 4132 Graves Hall - 333 W. 10th Avenue, Columbus, OH, 43210, USA

    Rolf F. Barth, Weilian Yang, Tianyao Huo & Robin Nakkula

  3. European Synchrotron Radiation Facility, ID17 Medical Beamline, 71 Avenue Martyrs, 38000, Grenoble, France

    Hélène Elleaume, Julia Rousseau & Laure Bobyk

  4. Service de Radiothérapie, Centre Hospitalier Universitaire Grenoble-Alpes, 38700, La Tronche, France

    Jacques Balosso

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  1. Hélène Elleaume
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All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All animal studies performed by Hélène Elleaume’s team were performed in compliance with the European Directive 2010/63/EU. The protocols were submitted to the ESRF ethical committee reference number ETHAX N°113. Animal studies carried out by Rolf Barth and his research team were in accordance with the Guide for the Care and the Use of Laboratory Animals (National Academy press, Washington DC, 1996) and the protocols were approved by the Institutional Laboratory Care and Use Committee of The Ohio State University.

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Elleaume, H., Barth, R.F., Rousseau, J. et al. Radiation therapy combined with intracerebral convection-enhanced delivery of cisplatin or carboplatin for treatment of the F98 rat glioma. J Neurooncol 149, 193–208 (2020). https://doi.org/10.1007/s11060-020-03600-x

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