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Published in: European Radiology 7/2007

01-07-2007 | Neuro

Predicting patterns of glioma recurrence using diffusion tensor imaging

Authors: Stephen J. Price, Rajesh Jena, Neil G. Burnet, T. Adrian Carpenter, John D. Pickard, Jonathan H. Gillard

Published in: European Radiology | Issue 7/2007

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Abstract

Although multimodality therapy for high-grade gliomas is making some improvement in outcome, most patients will still die from their disease within a short time. We need tools that allow treatments to be tailored to an individual. In this study we used diffusion tensor imaging (DTI), a technique sensitive to subtle disruption of white-matter tracts due to tumour infiltration, to see if it can be used to predict patterns of glioma recurrence. In this study we imaged 26 patients with gliomas using DTI. Patients were imaged after 2 years or on symptomatic tumour recurrence. The diffusion tensor was split into its isotropic (p) and anisotropic (q) components, and these were plotted on T2-weighted images to show the pattern of DTI abnormality. This was compared to the pattern of recurrence. Three DTI patterns could be identified: (a) a diffuse pattern of abnormality where p exceeded q in all directions and was associated with diffuse increase in tumour size; (b) a localised pattern of abnormality where the tumour recurred in one particular direction; and (c) a pattern of minimal abnormality seen in some patients with or without evidence of recurrence. Diffusion tensor imaging is able to predict patterns of tumour recurrence and may allow better individualisation of tumour management and stratification for randomised controlled trials.
Literature
1.
go back to reference Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJB, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996PubMedCrossRef Stupp R, Mason WP, van den Bent MJ, Weller M, Fisher B, Taphoorn MJB, Belanger K, Brandes AA, Marosi C, Bogdahn U, Curschmann J, Janzer RC, Ludwin SK, Gorlia T, Allgeier A, Lacombe D, Cairncross JG, Eisenhauer E, Mirimanoff RO (2005) Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N Engl J Med 352:987–996PubMedCrossRef
2.
go back to reference Coons SW, Johnson PC, Shapiro JR (1995) Cytogenetic and flow cytometry DNA analysis of regional heterogeneity in a low grade human glioma. Cancer Res 55:1569–1577PubMed Coons SW, Johnson PC, Shapiro JR (1995) Cytogenetic and flow cytometry DNA analysis of regional heterogeneity in a low grade human glioma. Cancer Res 55:1569–1577PubMed
3.
go back to reference Paulus W, Peiffer J (1989) Intratumoral histologic heterogeneity of gliomas. A quantitative study. Cancer 64:442–447PubMedCrossRef Paulus W, Peiffer J (1989) Intratumoral histologic heterogeneity of gliomas. A quantitative study. Cancer 64:442–447PubMedCrossRef
4.
5.
go back to reference Price SJ, Burnet NG, Donovan T, Green HA, Pena A, Antoun NM, Pickard JD, Carpenter TA, Gillard JH (2003) Diffusion tensor imaging of brain tumours at 3T: a potential tool for assessing white matter tract invasion? Clin Radiol 58:455–462PubMedCrossRef Price SJ, Burnet NG, Donovan T, Green HA, Pena A, Antoun NM, Pickard JD, Carpenter TA, Gillard JH (2003) Diffusion tensor imaging of brain tumours at 3T: a potential tool for assessing white matter tract invasion? Clin Radiol 58:455–462PubMedCrossRef
6.
go back to reference Provenzale JM, McGraw P, Mhatre P, Guo AC, Delong D (2004) Peritumoral brain regions in gliomas and meningiomas: investigation with isotropic diffusion-weighted MR imaging and diffusion-tensor MR imaging. Radiology 232:451–460PubMedCrossRef Provenzale JM, McGraw P, Mhatre P, Guo AC, Delong D (2004) Peritumoral brain regions in gliomas and meningiomas: investigation with isotropic diffusion-weighted MR imaging and diffusion-tensor MR imaging. Radiology 232:451–460PubMedCrossRef
7.
go back to reference Witwer BP, Moftakhar R, Hasan KM, Deshmukh P, Haughton V, Field A, Arfanakis K, Noyes J, Moritz CH, Meyerand ME, Rowley HA, Alexander AL, Badie B (2002) Diffusion-tensor imaging of white matter tracts in patients with cerebral neoplasm. J Neurosurg 97:568–575PubMedCrossRef Witwer BP, Moftakhar R, Hasan KM, Deshmukh P, Haughton V, Field A, Arfanakis K, Noyes J, Moritz CH, Meyerand ME, Rowley HA, Alexander AL, Badie B (2002) Diffusion-tensor imaging of white matter tracts in patients with cerebral neoplasm. J Neurosurg 97:568–575PubMedCrossRef
8.
go back to reference Field AS, Alexander AL, Wu YC, Hasan KM, Witwer B, Badie B (2004) Diffusion tensor eigenvector directional color imaging patterns in the evaluation of cerebral white matter tracts altered by tumor. J Magn Reson Imaging 20:555–562PubMedCrossRef Field AS, Alexander AL, Wu YC, Hasan KM, Witwer B, Badie B (2004) Diffusion tensor eigenvector directional color imaging patterns in the evaluation of cerebral white matter tracts altered by tumor. J Magn Reson Imaging 20:555–562PubMedCrossRef
9.
go back to reference Price SJ, Pena A, Burnet NG, Jena R, Green HA, Carpenter TA, Pickard JD, Gillard JH (2004) Tissue signature characterisation of diffusion tensor abnormalities in cerebral gliomas. Eur Radiol 14:1909–1917PubMedCrossRef Price SJ, Pena A, Burnet NG, Jena R, Green HA, Carpenter TA, Pickard JD, Gillard JH (2004) Tissue signature characterisation of diffusion tensor abnormalities in cerebral gliomas. Eur Radiol 14:1909–1917PubMedCrossRef
10.
go back to reference Price SJ, Jena R, Burnet NG, Hutchinson PJ, Dean AF, Pena A, Pickard JD, Carpenter TA, Gillard JH (2006) Improved delineation of glioma margins and regions of infiltration using diffusion tensor imaging: an image-guided biopsy study. AJNR Am J Neuroradiol 27(9):1969–1974PubMed Price SJ, Jena R, Burnet NG, Hutchinson PJ, Dean AF, Pena A, Pickard JD, Carpenter TA, Gillard JH (2006) Improved delineation of glioma margins and regions of infiltration using diffusion tensor imaging: an image-guided biopsy study. AJNR Am J Neuroradiol 27(9):1969–1974PubMed
11.
go back to reference Price SJ, Pena A, Burnet NG, Pickard JD, Gillard JH (2004) Detecting glioma invasion of the corpus callosum using diffusion tensor imaging. Br J Neurosurg 18:391–395PubMedCrossRef Price SJ, Pena A, Burnet NG, Pickard JD, Gillard JH (2004) Detecting glioma invasion of the corpus callosum using diffusion tensor imaging. Br J Neurosurg 18:391–395PubMedCrossRef
12.
go back to reference Basser PJ, Mattiello J, LeBihan D (1994) Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B 103:247–254PubMedCrossRef Basser PJ, Mattiello J, LeBihan D (1994) Estimation of the effective self-diffusion tensor from the NMR spin echo. J Magn Reson B 103:247–254PubMedCrossRef
14.
go back to reference Hochberg FH, Pruitt A (1980) Assumptions in the radiotherapy of glioblastoma. Neurology 30:907–911PubMed Hochberg FH, Pruitt A (1980) Assumptions in the radiotherapy of glioblastoma. Neurology 30:907–911PubMed
15.
go back to reference Albert FK, Forsting M, Sartor K, Adams HP, Kunze S (1994) Early postoperative magnetic resonance imaging after resection of malignant glioma: objective evaluation of residual tumor and its influence on regrowth and prognosis. Neurosurgery 34:45–60PubMedCrossRef Albert FK, Forsting M, Sartor K, Adams HP, Kunze S (1994) Early postoperative magnetic resonance imaging after resection of malignant glioma: objective evaluation of residual tumor and its influence on regrowth and prognosis. Neurosurgery 34:45–60PubMedCrossRef
16.
go back to reference Burger PC, Heinz ER, Shibata T, Kleihues P (1988) Topographic anatomy and CT correlations in the untreated glioblastoma multiforme. J Neurosurg 68:698–704PubMed Burger PC, Heinz ER, Shibata T, Kleihues P (1988) Topographic anatomy and CT correlations in the untreated glioblastoma multiforme. J Neurosurg 68:698–704PubMed
17.
go back to reference Burger PC, Dubois PJ, Schold SC Jr, Smith KR Jr, Odom GL, Crafts DC, Giangaspero F (1983) Computerized tomographic and pathologic studies of the untreated, quiescent, and recurrent glioblastoma multiforme. J Neurosurg 58:159–169PubMed Burger PC, Dubois PJ, Schold SC Jr, Smith KR Jr, Odom GL, Crafts DC, Giangaspero F (1983) Computerized tomographic and pathologic studies of the untreated, quiescent, and recurrent glioblastoma multiforme. J Neurosurg 58:159–169PubMed
18.
go back to reference Kelly PJ, Daumas-Duport C, Kispert DB, Kall BA, Scheithauer BW, Illig JJ (1987) Imaging-based stereotaxic serial biopsies in untreated intracranial glial neoplasms. J Neurosurg 66:865–874PubMed Kelly PJ, Daumas-Duport C, Kispert DB, Kall BA, Scheithauer BW, Illig JJ (1987) Imaging-based stereotaxic serial biopsies in untreated intracranial glial neoplasms. J Neurosurg 66:865–874PubMed
19.
go back to reference Silbergeld DL, Chicoine MR (1997) Isolation and characterization of human malignant glioma cells from histologically normal brain. J Neurosurg 86:525–531PubMedCrossRef Silbergeld DL, Chicoine MR (1997) Isolation and characterization of human malignant glioma cells from histologically normal brain. J Neurosurg 86:525–531PubMedCrossRef
20.
go back to reference Emami B, Lyman J, Brown A, Coia L, Goitein M, Munzenrider JE, Shank B, Solin LJ, Wesson M (1991) Tolerance of normal tissue to therapeutic irradiation. Int J Radiat Oncol Biol Phys 21:109–122PubMed Emami B, Lyman J, Brown A, Coia L, Goitein M, Munzenrider JE, Shank B, Solin LJ, Wesson M (1991) Tolerance of normal tissue to therapeutic irradiation. Int J Radiat Oncol Biol Phys 21:109–122PubMed
21.
go back to reference Lee SW, Fraass BA, Marsh LH, Herbort K, Gebarski SS, Martel MK, Radany EH, Lichter AS, Sandler HM (1999) Patterns of failure following high-dose 3-D conformal radiotherapy for high-grade astrocytomas: a quantitative dosimetric study. Int J Radiat Oncol Biol Phys 43:79–88PubMed Lee SW, Fraass BA, Marsh LH, Herbort K, Gebarski SS, Martel MK, Radany EH, Lichter AS, Sandler HM (1999) Patterns of failure following high-dose 3-D conformal radiotherapy for high-grade astrocytomas: a quantitative dosimetric study. Int J Radiat Oncol Biol Phys 43:79–88PubMed
22.
go back to reference Oppitz U, Maessen D, Zunterer H, Richter S, Flentje M (1999) 3D-recurrence-patterns of glioblastomas after CT-planned postoperative irradiation. Radiother Oncol 53:53–57PubMedCrossRef Oppitz U, Maessen D, Zunterer H, Richter S, Flentje M (1999) 3D-recurrence-patterns of glioblastomas after CT-planned postoperative irradiation. Radiother Oncol 53:53–57PubMedCrossRef
23.
go back to reference Fitzek MM, Thornton AF, Rabinov JD, Lev MH, Pardo FS, Munzenrider JE, Okunieff P, Bussiere M, Braun I, Hochberg FH, Hedley-Whyte ET, Liebsch NJ, Harsh GR (1999) Accelerated fractionated proton/photon irradiation to 90 cobalt gray equivalent for glioblastoma multiforme: results of a phase II prospective trial. J Neurosurg 91:251–260PubMed Fitzek MM, Thornton AF, Rabinov JD, Lev MH, Pardo FS, Munzenrider JE, Okunieff P, Bussiere M, Braun I, Hochberg FH, Hedley-Whyte ET, Liebsch NJ, Harsh GR (1999) Accelerated fractionated proton/photon irradiation to 90 cobalt gray equivalent for glioblastoma multiforme: results of a phase II prospective trial. J Neurosurg 91:251–260PubMed
24.
go back to reference Pirzkall A, Li X, Oh J, Chang S, Berger MS, Larson DA, Verhey LJ, Dillon WP, Nelson SJ (2004) 3D MRSI for resected high-grade gliomas before RT: tumor extent according to metabolic activity in relation to MRI. Int J Radiat Oncol Biol Phys 59:126–137PubMedCrossRef Pirzkall A, Li X, Oh J, Chang S, Berger MS, Larson DA, Verhey LJ, Dillon WP, Nelson SJ (2004) 3D MRSI for resected high-grade gliomas before RT: tumor extent according to metabolic activity in relation to MRI. Int J Radiat Oncol Biol Phys 59:126–137PubMedCrossRef
25.
go back to reference Jena R, Price SJ, Baker C, Jefferies SJ, Pickard JD, Gillard JH, Burnet NG (2005) Diffusion tensor imaging: possible implications for radiotherapy treatment planning of patients with high-grade glioma. Clin Oncol 17:581–590CrossRef Jena R, Price SJ, Baker C, Jefferies SJ, Pickard JD, Gillard JH, Burnet NG (2005) Diffusion tensor imaging: possible implications for radiotherapy treatment planning of patients with high-grade glioma. Clin Oncol 17:581–590CrossRef
26.
go back to reference Grosu AL, Weber WA, Riedel E, Jeremic B, Nieder C, Franz M, Gumprecht H, Jaeger R, Schwaiger M, Molls M (2005) L-(methyl-11C) methionine positron emission tomography for target delineation in resected high-grade gliomas before radiotherapy. Int J Radiat Oncol Biol Phys 63:64–74PubMedCrossRef Grosu AL, Weber WA, Riedel E, Jeremic B, Nieder C, Franz M, Gumprecht H, Jaeger R, Schwaiger M, Molls M (2005) L-(methyl-11C) methionine positron emission tomography for target delineation in resected high-grade gliomas before radiotherapy. Int J Radiat Oncol Biol Phys 63:64–74PubMedCrossRef
27.
go back to reference Ekinci G, Akpinar IN, Baltacioglu F, Erzen C, Kilic T, Elmaci I, Pamir N (2003) Early-postoperative magnetic resonance imaging in glial tumors: prediction of tumor regrowth and recurrence. Eur J Radiol 45:99–107PubMedCrossRef Ekinci G, Akpinar IN, Baltacioglu F, Erzen C, Kilic T, Elmaci I, Pamir N (2003) Early-postoperative magnetic resonance imaging in glial tumors: prediction of tumor regrowth and recurrence. Eur J Radiol 45:99–107PubMedCrossRef
28.
go back to reference Pope WB, Sayre J, Perlina A, Villablanca JP, Mischel PS, Cloughesy TF (2005) MR imaging correlates of survival in patients with high-grade gliomas. AJNR Am J Neuroradiol 26:2466–2474PubMed Pope WB, Sayre J, Perlina A, Villablanca JP, Mischel PS, Cloughesy TF (2005) MR imaging correlates of survival in patients with high-grade gliomas. AJNR Am J Neuroradiol 26:2466–2474PubMed
29.
go back to reference Mineura K, Sasajima T, Kowada M, Ogawa T, Hatazawa J, Shishido F, Uemura K (1994) Perfusion and metabolism in predicting the survival of patients with cerebral gliomas. Cancer 73:2386–2394PubMedCrossRef Mineura K, Sasajima T, Kowada M, Ogawa T, Hatazawa J, Shishido F, Uemura K (1994) Perfusion and metabolism in predicting the survival of patients with cerebral gliomas. Cancer 73:2386–2394PubMedCrossRef
30.
go back to reference Cao Y, Tsien CI, Nagesh V, Junck L, Ten Haken R, Ross BD, Chenevert TL, Lawrence TS (2006) Clinical investigation survival prediction in high-grade gliomas by MRI perfusion before and during early stage of RT. Int J Radiat Oncol Biol Phys 64:876–885PubMedCrossRef Cao Y, Tsien CI, Nagesh V, Junck L, Ten Haken R, Ross BD, Chenevert TL, Lawrence TS (2006) Clinical investigation survival prediction in high-grade gliomas by MRI perfusion before and during early stage of RT. Int J Radiat Oncol Biol Phys 64:876–885PubMedCrossRef
31.
go back to reference De Witte O, Goldberg I, Wikler D, Rorive S, Damhaut P, Monclus M, Salmon I, Brotchi J, Goldman S (2001) Positron emission tomography with injection of methionine as a prognostic factor in glioma. J Neurosurg 95:746–750PubMedCrossRef De Witte O, Goldberg I, Wikler D, Rorive S, Damhaut P, Monclus M, Salmon I, Brotchi J, Goldman S (2001) Positron emission tomography with injection of methionine as a prognostic factor in glioma. J Neurosurg 95:746–750PubMedCrossRef
32.
go back to reference Johnson PC, Hunt SJ, Drayer BP (1989) Human cerebral gliomas: correlation of postmortem MR imaging and neuropathologic findings. Radiology 170:211–217PubMed Johnson PC, Hunt SJ, Drayer BP (1989) Human cerebral gliomas: correlation of postmortem MR imaging and neuropathologic findings. Radiology 170:211–217PubMed
33.
go back to reference Sathy BN, Hsu Y-H, Jang T, Recht L, Chang C (2006) Development and evolution of glioma after ENU exposure: a model of malignant transformation of low grade gliomas. Proc Intl Soc Mag Reson Med 14:613 Sathy BN, Hsu Y-H, Jang T, Recht L, Chang C (2006) Development and evolution of glioma after ENU exposure: a model of malignant transformation of low grade gliomas. Proc Intl Soc Mag Reson Med 14:613
34.
go back to reference Sinha S, Bastin ME, Wardlaw JM, Armitage PA, Whittle IR (2004) Effects of dexamethasone on peritumoural oedematous brain: a DT-MRI study. J Neurol Neurosurg Psychiatry 75:1632–1635CrossRef Sinha S, Bastin ME, Wardlaw JM, Armitage PA, Whittle IR (2004) Effects of dexamethasone on peritumoural oedematous brain: a DT-MRI study. J Neurol Neurosurg Psychiatry 75:1632–1635CrossRef
Metadata
Title
Predicting patterns of glioma recurrence using diffusion tensor imaging
Authors
Stephen J. Price
Rajesh Jena
Neil G. Burnet
T. Adrian Carpenter
John D. Pickard
Jonathan H. Gillard
Publication date
01-07-2007
Publisher
Springer-Verlag
Published in
European Radiology / Issue 7/2007
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-006-0561-2

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