Journal Article
. 2014 Aug; 90(2):446-53.
doi: 10.1016/j.ijrobp.2014.06.015.

Toward distinguishing recurrent tumor from radiation necrosis: DWI and MTC in a Gamma Knife--irradiated mouse glioma model

Carlos J Perez-Torres 1 John A Engelbach 1 Jeremy Cates 2 Dinesh Thotala 2 Liya Yuan 3 Robert E Schmidt 4 Keith M Rich 5 Robert E Drzymala 2 Joseph J H Ackerman 6 Joel R Garbow 7 
Affiliations
  • PMID: 25104071
  •     32 References
  •     12 citations

Abstract

Purpose: Accurate noninvasive diagnosis is vital for effective treatment planning. Presently, standard anatomical magnetic resonance imaging (MRI) is incapable of differentiating recurring tumor from delayed radiation injury, as both lesions are hyperintense in both postcontrast T1- and T2-weighted images. Further studies are therefore necessary to identify an MRI paradigm that can differentially diagnose these pathologies. Mouse glioma and radiation injury models provide a powerful platform for this purpose.

Methods And Materials: Two MRI contrasts that are widely used in the clinic were chosen for application to a glioma/radiation-injury model: diffusion weighted imaging, from which the apparent diffusion coefficient (ADC) is obtained, and magnetization transfer contrast, from which the magnetization transfer ratio (MTR) is obtained. These metrics were evaluated longitudinally, first in each lesion type alone-glioma versus irradiation - and then in a combined irradiated glioma model.

Results: MTR was found to be consistently decreased in all lesions compared to nonlesion brain tissue (contralateral hemisphere), with limited specificity between lesion types. In contrast, ADC, though less sensitive to the presence of pathology, was increased in radiation injury and decreased in tumors. In the irradiated glioma model, ADC also increased immediately after irradiation, but decreased as the tumor regrew.

Conclusions: ADC is a better metric than MTR for differentiating glioma from radiation injury. However, MTR was more sensitive to both tumor and radiation injury than ADC, suggesting a possible role in detecting lesions that do not enhance strongly on T1-weighted images.

Magnetization transfer analysis of brain tumor, infection, and infarction.
M H Pui.
J Magn Reson Imaging, 2000 Sep 19; 12(3). PMID: 10992306
MR classification of brain gliomas: value of magnetization transfer and conventional imaging.
T Kurki, N Lundbom, H Kalimo, S Valtonen.
Magn Reson Imaging, 1995 Jan 01; 13(4). PMID: 7674845
Diffusion-weighted MR imaging in pancreatic endocrine tumors correlated with histopathologic characteristics.
Yi Wang, Zongming E Chen, +4 authors, Frank H Miller.
J Magn Reson Imaging, 2011 Apr 22; 33(5). PMID: 21509863
Usefulness of diffusion-weighted MRI with echo-planar technique in the evaluation of cellularity in gliomas.
T Sugahara, Y Korogi, +9 authors, M Takahashi.
J Magn Reson Imaging, 1999 Feb 25; 9(1). PMID: 10030650
Highly Cited.
Relationships between choline magnetic resonance spectroscopy, apparent diffusion coefficient and quantitative histopathology in human glioma.
R K Gupta, T F Cloughesy, +7 authors, J R Alger.
J Neurooncol, 2001 Mar 27; 50(3). PMID: 11263501
A GSK-3β inhibitor protects against radiation necrosis in mouse brain.
Xiaoyu Jiang, Carlos J Perez-Torres, +10 authors, Joel R Garbow.
Int J Radiat Oncol Biol Phys, 2014 Jun 28; 89(4). PMID: 24969790    Free PMC article.
Gliomas in rodent whisker barrel cortex: a new tumor model.
E W Sherburn, J E Wanebo, +3 authors, T A Woolsey.
J Neurosurg, 1999 Nov 30; 91(5). PMID: 10541239
Evaluating pediatric brain tumor cellularity with diffusion-tensor imaging.
K M Gauvain, R C McKinstry, +4 authors, R J Hayashi.
AJR Am J Roentgenol, 2001 Jul 20; 177(2). PMID: 11461881
Correlation of the apparent diffusion coefficiency values on diffusion-weighted imaging with prognostic factors for breast cancer.
S Y Choi, Y-W Chang, +3 authors, D Y Seo.
Br J Radiol, 2011 Dec 01; 85(1016). PMID: 22128125    Free PMC article.
Permeability estimates in histopathology-proved treatment-induced necrosis using perfusion CT: can these add to other perfusion parameters in differentiating from recurrent/progressive tumors?
R Jain, J Narang, +7 authors, T Mikkelsen.
AJNR Am J Neuroradiol, 2011 Feb 19; 32(4). PMID: 21330392    Free PMC article.
Cerebral radiation necrosis simulating a brain tumor. Case report.
E F Eyster, S L Nielsen, G E Sheline, C B Wilson.
J Neurosurg, 1974 Feb 01; 40(2). PMID: 4203210
Brain tumors induced with Rous sarcoma virus, Schmidt-Ruppin strain. I. Induction of brain tumors in adult mice with Rous chicken sarcoma cells.
T Kumanishi.
Jpn J Exp Med, 1967 Oct 01; 37(5). PMID: 4301953
Glioma residual or recurrence versus radiation necrosis: accuracy of pentavalent technetium-99m-dimercaptosuccinic acid [Tc-99m (V) DMSA] brain SPECT compared to proton magnetic resonance spectroscopy (1H-MRS): initial results.
Amr Amin, Hosna Moustafa, Ebaa Ahmed, Mohamed El-Toukhy.
J Neurooncol, 2011 Sep 14; 106(3). PMID: 21912937
Radiation-induced brain injury: A review.
Dana Greene-Schloesser, Mike E Robbins, +3 authors, Michael D Chan.
Front Oncol, 2012 Jul 27; 2. PMID: 22833841    Free PMC article.
Highly Cited.
Mechanisms of radiation injury to the central nervous system: implications for neuroprotection.
C Shun Wong, Albert J Van der Kogel.
Mol Interv, 2004 Oct 09; 4(5). PMID: 15471910
Review.
Radiation necrosis in the brain: imaging features and differentiation from tumor recurrence.
Ritu Shah, Surjith Vattoth, +5 authors, Joel K Curé.
Radiographics, 2012 Sep 15; 32(5). PMID: 22977022
The characterization of human brain tumor using magnetization transfer technique in magnetic resonance imaging.
A Okumura, K Takenaka, +4 authors, S Era.
Neurol Res, 1999 May 13; 21(3). PMID: 10319332
Glioma recurrence versus radiation necrosis? A pilot comparison of arterial spin-labeled, dynamic susceptibility contrast enhanced MRI, and FDG-PET imaging.
Yelda Ozsunar, Mark E Mullins, +5 authors, Michael H Lev.
Acad Radiol, 2010 Jan 12; 17(3). PMID: 20060750
Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma.
Roger Stupp, Warren P Mason, +18 authors, National Cancer Institute of Canada Clinical Trials Group.
N Engl J Med, 2005 Mar 11; 352(10). PMID: 15758009
Highly Cited.
Radiation necrosis following treatment of high grade glioma--a review of the literature and current understanding.
Alan Siu, Joshua J Wind, +3 authors, Jonathan H Sherman.
Acta Neurochir (Wien), 2011 Dec 02; 154(2). PMID: 22130634
Review.
Effects of radiotherapy with concomitant and adjuvant temozolomide versus radiotherapy alone on survival in glioblastoma in a randomised phase III study: 5-year analysis of the EORTC-NCIC trial.
Roger Stupp, Monika E Hegi, +23 authors, National Cancer Institute of Canada Clinical Trials Group.
Lancet Oncol, 2009 Mar 10; 10(5). PMID: 19269895
Highly Cited.
Assessment of MRI parameters as imaging biomarkers for radiation necrosis in the rat brain.
Silun Wang, Erik Tryggestad, +6 authors, Jinyuan Zhou.
Int J Radiat Oncol Biol Phys, 2012 Apr 10; 83(3). PMID: 22483739    Free PMC article.
Malignant gliomas: MR imaging spectrum of radiation therapy- and chemotherapy-induced necrosis of the brain after treatment.
A J Kumar, N E Leeds, +4 authors, V A Levin.
Radiology, 2000 Nov 04; 217(2). PMID: 11058631
Highly Cited.
Cerebral radiation necrosis: a review of the pathobiology, diagnosis and management considerations.
Gazanfar Rahmathulla, Nicholas F Marko, Robert J Weil.
J Clin Neurosci, 2013 Feb 19; 20(4). PMID: 23416129
Review.
Anti-VEGF antibodies mitigate the development of radiation necrosis in mouse brain.
Xiaoyu Jiang, John A Engelbach, +8 authors, Joel R Garbow.
Clin Cancer Res, 2014 Mar 22; 20(10). PMID: 24647570    Free PMC article.
Utility of apparent diffusion coefficient in predicting the outcome of Gamma Knife-treated brain metastases prior to changes in tumor volume: a preliminary study.
Marc Goldman, Jerrold L Boxerman, Jeffrey M Rogg, Georg Norén.
J Neurosurg, 2006 Dec 01; 105 Suppl. PMID: 18503353
Characterization of brain tumors by MRS, DWI and Ki-67 labeling index.
J A Calvar, F J Meli, +6 authors, G Sevlever.
J Neurooncol, 2005 Jun 07; 72(3). PMID: 15937653
Distinction between recurrent glioma and radiation injury using magnetic resonance spectroscopy in combination with diffusion-weighted imaging.
Qing-Shi Zeng, Chuan-Fu Li, +2 authors, De-Chao Feng.
Int J Radiat Oncol Biol Phys, 2007 Feb 10; 68(1). PMID: 17289287
Differentiation of recurrent glioblastoma multiforme from radiation necrosis after external beam radiation therapy with dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging.
Ramon F Barajas, Jamie S Chang, +4 authors, Soonmee Cha.
Radiology, 2009 Oct 01; 253(2). PMID: 19789240    Free PMC article.
Highly Cited.
Discriminating radiation necrosis from tumor progression in gliomas: a systematic review what is the best imaging modality?
Ashish H Shah, Brian Snelling, +5 authors, Ricardo J Komotar.
J Neurooncol, 2013 Jan 25; 112(2). PMID: 23344789
Systematic Review.
Conventional MRI does not reliably distinguish radiation necrosis from tumor recurrence after stereotactic radiosurgery.
Abigail L Stockham, Andrew L Tievsky, +5 authors, Samuel T Chao.
J Neurooncol, 2012 May 29; 109(1). PMID: 22638727
Status quo--standard-of-care medical and radiation therapy for glioblastoma.
Kevin P Becker, James Yu.
Cancer J, 2012 Feb 01; 18(1). PMID: 22290252
Review.
Perilesional edema in radiation necrosis reflects axonal degeneration.
Carlos J Perez-Torres, Liya Yuan, +3 authors, Joel R Garbow.
Radiat Oncol, 2015 Feb 01; 10. PMID: 25636531    Free PMC article.
Specificity of vascular endothelial growth factor treatment for radiation necrosis.
Carlos J Perez-Torres, Liya Yuan, +5 authors, Joel R Garbow.
Radiother Oncol, 2015 Sep 17; 117(2). PMID: 26376163    Free PMC article.
A Gamma-Knife-Enabled Mouse Model of Cerebral Single-Hemisphere Delayed Radiation Necrosis.
Xiaoyu Jiang, Liya Yuan, +10 authors, Joel R Garbow.
PLoS One, 2015 Oct 07; 10(10). PMID: 26440791    Free PMC article.
A preclinical murine model for the early detection of radiation-induced brain injury using magnetic resonance imaging and behavioral tests for learning and memory: with applications for the evaluation of possible stem cell imaging agents and therapies.
Ethel J Ngen, Lee Wang, +6 authors, Dmitri Artemov.
J Neurooncol, 2016 Mar 30; 128(2). PMID: 27021492
A comparative assessment of preclinical chemotherapeutic response of tumors using quantitative non-Gaussian diffusion MRI.
Junzhong Xu, Ke Li, +6 authors, John C Gore.
Magn Reson Imaging, 2016 Dec 07; 37. PMID: 27919785    Free PMC article.
The effect of radiation dose on the onset and progression of radiation-induced brain necrosis in the rat model.
Brad A Hartl, Htet S W Ma, +4 authors, Laura Marcu.
Int J Radiat Biol, 2017 Mar 18; 93(7). PMID: 28306402    Free PMC article.
Can anti-vascular endothelial growth factor antibody reverse radiation necrosis? A preclinical investigation.
Chong Duan, Carlos J Perez-Torres, +7 authors, Joel R Garbow.
J Neurooncol, 2017 Apr 21; 133(1). PMID: 28425047    Free PMC article.
Preclinical MRI: Studies of the irradiated brain.
Joel R Garbow, Christina I Tsien, Scott C Beeman.
J Magn Reson, 2018 May 01; 292. PMID: 29705034    Free PMC article.
Magnetic resonance imaging-guided radiation therapy using animal models of glioblastoma.
Christian Vanhove, Ingeborg Goethals.
Br J Radiol, 2018 Dec 20; 92(1095). PMID: 30563357    Free PMC article.
Review.
Impact of mouse strain and sex when modeling radiation necrosis.
Andrew J Boria, Carlos J Perez-Torres.
Radiat Oncol, 2020 Jun 05; 15(1). PMID: 32493371    Free PMC article.
Minimal difference between fractionated and single-fraction exposure in a murine model of radiation necrosis.
Andrew J Boria, Carlos J Perez-Torres.
Radiat Oncol, 2019 Aug 15; 14(1). PMID: 31409408    Free PMC article.
Dynamic Three-Dimensional ADC Changes of Parotid Glands During Radiotherapy Predict the Salivary Secretary Function in Patients With Head and Neck Squamous Carcinoma.
Mei Feng, Qingping Yin, +7 authors, Jinyi Lang.
Front Oncol, 2021 May 01; 11. PMID: 33928037    Free PMC article.