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Published in: Journal of Neuro-Oncology 3/2009

01-02-2009 | Clinical study - patient study

Relationship of pre-surgery metabolic and physiological MR imaging parameters to survival for patients with untreated GBM

Authors: Forrest W. Crawford, Inas S. Khayal, Colleen McGue, Suja Saraswathy, Andrea Pirzkall, Soonmee Cha, Kathleen R. Lamborn, Susan M. Chang, Mitchel S. Berger, Sarah J. Nelson

Published in: Journal of Neuro-Oncology | Issue 3/2009

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Abstract

Glioblastoma Multiforme (GBM) are heterogeneous lesions, both in terms of their appearance on anatomic images and their response to therapy. The goal of this study was to evaluate the prognostic value of parameters derived from physiological and metabolic images of these lesions. Fifty-six patients with GBM were scanned immediately before surgical resection using conventional anatomical MR imaging and, where possible, perfusion-weighted imaging, diffusion-weighted imaging, and proton MR spectroscopic imaging. The median survival time was 517 days, with 15 patients censored. Absolute anatomic lesion volumes were not associated with survival but patients for whom the combined volume of contrast enhancement and necrosis was a large percentage of the T2 hyperintense lesion had relatively poor survival. Other volumetric parameters linked with less favorable survival were the volume of the region with elevated choline to N-acetylaspartate index (CNI) and the volume within the T2 lesion that had apparent diffusion coefficient (ADC) less than 1.5 times that in white matter. Intensity parameters associated with survival were the maximum and the sum of levels of lactate and of lipid within the CNI lesion, as well as the magnitude of the 10th percentile of the normalized ADC within the contrast-enhancing lesion. Patients whose imaging parameters indicating that lesions with a relatively large percentage with breakdown of the blood brain barrier or necrosis, large regions with abnormal metabolism or areas with restricted diffusion have relatively poor survival. These parameters may provide useful information for predicting outcome and for the stratification of patients into high or low risk groups for clinical trials.
Literature
1.
go back to reference Oh J, Henry RG, Pirzkall A, Lu Y, Li X, Catalaa I et al (2004) Survival analysis in patients with glioblastoma multiforme: predictive value of choline-to-N-acetylaspartate index, apparent diffusion coefficient, and relative cerebral blood volume. J Magn Reson Imaging 19:546–554. doi:10.1002/jmri.20039 PubMedCrossRef Oh J, Henry RG, Pirzkall A, Lu Y, Li X, Catalaa I et al (2004) Survival analysis in patients with glioblastoma multiforme: predictive value of choline-to-N-acetylaspartate index, apparent diffusion coefficient, and relative cerebral blood volume. J Magn Reson Imaging 19:546–554. doi:10.​1002/​jmri.​20039 PubMedCrossRef
3.
go back to reference Simpson JR, Horton J, Scott C, Curran WJ, Rubin P, Fischbach J et al (1993) Influence of location and extent of surgical resection on survival of patients with glioblastoma multiforme: results of three consecutive Radiation Therapy Oncology Group (RTOG) clinical trials. Int J Radiat Oncol Biol Phys 26:239–244PubMed Simpson JR, Horton J, Scott C, Curran WJ, Rubin P, Fischbach J et al (1993) Influence of location and extent of surgical resection on survival of patients with glioblastoma multiforme: results of three consecutive Radiation Therapy Oncology Group (RTOG) clinical trials. Int J Radiat Oncol Biol Phys 26:239–244PubMed
4.
go back to reference Kowalczuk A, Macdonald RL, Amidei C, Dohrmann G 3rd, Erickson RK, Hekmatpanah J et al (1997) Quantitative imaging study of extent of surgical resection and prognosis of malignant astrocytomas. Neurosurgery 41:1028–1036. doi:10.1097/00006123-199711000-00004 (discussion 1036–1038)PubMedCrossRef Kowalczuk A, Macdonald RL, Amidei C, Dohrmann G 3rd, Erickson RK, Hekmatpanah J et al (1997) Quantitative imaging study of extent of surgical resection and prognosis of malignant astrocytomas. Neurosurgery 41:1028–1036. doi:10.​1097/​00006123-199711000-00004 (discussion 1036–1038)PubMedCrossRef
5.
go back to reference Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, De Monte F et al (2001) A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 95:190–198PubMed Lacroix M, Abi-Said D, Fourney DR, Gokaslan ZL, Shi W, De Monte F et al (2001) A multivariate analysis of 416 patients with glioblastoma multiforme: prognosis, extent of resection, and survival. J Neurosurg 95:190–198PubMed
11.
go back to reference McKnight TR, von dem Bussche MH, Vigneron DB, Lu Y, Berger MS, McDermott MW et al (2002) Histopathological validation of a three-dimensional magnetic resonance spectroscopy index as a predictor of tumor presence. J Neurosurg 97:794–802PubMed McKnight TR, von dem Bussche MH, Vigneron DB, Lu Y, Berger MS, McDermott MW et al (2002) Histopathological validation of a three-dimensional magnetic resonance spectroscopy index as a predictor of tumor presence. J Neurosurg 97:794–802PubMed
12.
go back to reference Pirzkall A, Li X, Oh J, Chang S, Berger MS, Larson DA et al (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 59:126–137. doi:10.1016/j.ijrobp.2003.08.023 PubMed Pirzkall A, Li X, Oh J, Chang S, Berger MS, Larson DA et al (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 59:126–137. doi:10.​1016/​j.​ijrobp.​2003.​08.​023 PubMed
13.
go back to reference Chen J, Xia J, Zhou YC, Xia LM, Zhu WZ, Zou ML et al (2005) Correlation between magnetic resonance diffusion weighted imaging and cell density in astrocytoma. Zhonghua Zhong Liu Za Zhi 27:309–311PubMed Chen J, Xia J, Zhou YC, Xia LM, Zhu WZ, Zou ML et al (2005) Correlation between magnetic resonance diffusion weighted imaging and cell density in astrocytoma. Zhonghua Zhong Liu Za Zhi 27:309–311PubMed
14.
go back to reference Fuss M, Wenz F, Essig M, Muenter M, Debus J, Herman TS et al (2001) Tumor angiogenesis of low-grade astrocytomas measured by dynamic susceptibility contrast-enhanced MRI (DSC-MRI) is predictive of local tumor control after radiation therapy. Int J Radiat Oncol Biol Phys 51:478–482. doi:10.1016/S0360-3016(01)01691-1 PubMed Fuss M, Wenz F, Essig M, Muenter M, Debus J, Herman TS et al (2001) Tumor angiogenesis of low-grade astrocytomas measured by dynamic susceptibility contrast-enhanced MRI (DSC-MRI) is predictive of local tumor control after radiation therapy. Int J Radiat Oncol Biol Phys 51:478–482. doi:10.​1016/​S0360-3016(01)01691-1 PubMed
16.
go back to reference Chenevert TL, Stegman LD, Taylor JM, Robertson PL, Greenberg HS, Rehemtulla A et al (2000) Diffusion magnetic resonance imaging: an early surrogate marker of therapeutic efficacy in brain tumors. J Natl Cancer Inst 92:2029–2036. doi:10.1093/jnci/92.24.2029 PubMedCrossRef Chenevert TL, Stegman LD, Taylor JM, Robertson PL, Greenberg HS, Rehemtulla A et al (2000) Diffusion magnetic resonance imaging: an early surrogate marker of therapeutic efficacy in brain tumors. J Natl Cancer Inst 92:2029–2036. doi:10.​1093/​jnci/​92.​24.​2029 PubMedCrossRef
17.
go back to reference Kono K, Inoue Y, Nakayama K, Shakudo M, Morino M, Ohata K et al (2001) The role of diffusion-weighted imaging in patients with brain tumors. AJNR Am J Neuroradiol 22:1081–1088PubMed Kono K, Inoue Y, Nakayama K, Shakudo M, Morino M, Ohata K et al (2001) The role of diffusion-weighted imaging in patients with brain tumors. AJNR Am J Neuroradiol 22:1081–1088PubMed
18.
go back to reference Sugahara T, Korogi Y, Kochi M, Ikushima I, Shigematu Y, Hirai T et al (1999) Usefulness of diffusion-weighted MRI with echo-planar technique in the evaluation of cellularity in gliomas. J Magn Reson Imaging 9:53–60. doi:10.1002/(SICI)1522-2586(199901)9:1<53::AID-JMRI7>3.0.CO;2-2PubMedCrossRef Sugahara T, Korogi Y, Kochi M, Ikushima I, Shigematu Y, Hirai T et al (1999) Usefulness of diffusion-weighted MRI with echo-planar technique in the evaluation of cellularity in gliomas. J Magn Reson Imaging 9:53–60. doi:10.1002/(SICI)1522-2586(199901)9:1<53::AID-JMRI7>3.0.CO;2-2PubMedCrossRef
19.
go back to reference Mardor Y, Pfeffer R, Spiegelmann R, Roth Y, Maier SE, Nissim O et al (2003) Early detection of response to radiation therapy in patients with brain malignancies using conventional and high b-value diffusion-weighted magnetic resonance imaging. J Clin Oncol 21:1094–1100. doi:10.1200/JCO.2003.05.069 PubMedCrossRef Mardor Y, Pfeffer R, Spiegelmann R, Roth Y, Maier SE, Nissim O et al (2003) Early detection of response to radiation therapy in patients with brain malignancies using conventional and high b-value diffusion-weighted magnetic resonance imaging. J Clin Oncol 21:1094–1100. doi:10.​1200/​JCO.​2003.​05.​069 PubMedCrossRef
21.
go back to reference Tarnawski R, Sokol M, Pieniazek P, Maciejewski B, Walecki J, Miszczyk L et al (2002) 1H-MRS in vivo predicts the early treatment outcome of postoperative radiotherapy for malignant gliomas. Int J Radiat Oncol Biol Phys 52:1271–1276. doi:10.1016/S0360-3016(01)02769-9 PubMedCrossRef Tarnawski R, Sokol M, Pieniazek P, Maciejewski B, Walecki J, Miszczyk L et al (2002) 1H-MRS in vivo predicts the early treatment outcome of postoperative radiotherapy for malignant gliomas. Int J Radiat Oncol Biol Phys 52:1271–1276. doi:10.​1016/​S0360-3016(01)02769-9 PubMedCrossRef
22.
go back to reference Li X, Jin H, Lu Y, Oh J, Chang S, Nelson SJ (2004) Identification of MRI and 1H MRSI parameters that may predict survival for patients with malignant gliomas. NMR Biomed 17:10–20. doi:10.1002/nbm.858 PubMedCrossRef Li X, Jin H, Lu Y, Oh J, Chang S, Nelson SJ (2004) Identification of MRI and 1H MRSI parameters that may predict survival for patients with malignant gliomas. NMR Biomed 17:10–20. doi:10.​1002/​nbm.​858 PubMedCrossRef
23.
go back to reference Barker FG 2nd, Prados MD, Chang SM, Gutin PH, Lamborn KR, Larson DA et al (1996) Radiation response and survival time in patients with glioblastoma multiforme. J Neurosurg 84:442–448PubMed Barker FG 2nd, Prados MD, Chang SM, Gutin PH, Lamborn KR, Larson DA et al (1996) Radiation response and survival time in patients with glioblastoma multiforme. J Neurosurg 84:442–448PubMed
24.
go back to reference Gamburg ES, Regine WF, Patchell RA, Strottmann JM, Mohiuddin M, Young AB (2000) The prognostic significance of midline shift at presentation on survival in patients with glioblastoma multiforme. Int J Radiat Oncol Biol Phys 48:1359–1362. doi:10.1016/S0360-3016(00)01410-3 PubMed Gamburg ES, Regine WF, Patchell RA, Strottmann JM, Mohiuddin M, Young AB (2000) The prognostic significance of midline shift at presentation on survival in patients with glioblastoma multiforme. Int J Radiat Oncol Biol Phys 48:1359–1362. doi:10.​1016/​S0360-3016(00)01410-3 PubMed
25.
go back to reference Keles GE, Lamborn KR, Chang SM, Prados MD, Berger MS (2004) Volume of residual disease as a predictor of outcome in adult patients with recurrent supratentorial glioblastomas multiforme who are undergoing chemotherapy. J Neurosurg 100:41–46PubMedCrossRef Keles GE, Lamborn KR, Chang SM, Prados MD, Berger MS (2004) Volume of residual disease as a predictor of outcome in adult patients with recurrent supratentorial glioblastomas multiforme who are undergoing chemotherapy. J Neurosurg 100:41–46PubMedCrossRef
26.
go back to reference Kreth FW, Berlis A, Spiropoulou V, Faist M, Scheremet R, Rossner R et al (1999) The role of tumor resection in the treatment of glioblastoma multiforme in adults. Cancer 86:2117–2123. doi:10.1002/(SICI)1097-0142(19991115)86:10<2117::AID-CNCR33>3.0.CO;2-8PubMedCrossRef Kreth FW, Berlis A, Spiropoulou V, Faist M, Scheremet R, Rossner R et al (1999) The role of tumor resection in the treatment of glioblastoma multiforme in adults. Cancer 86:2117–2123. doi:10.1002/(SICI)1097-0142(19991115)86:10<2117::AID-CNCR33>3.0.CO;2-8PubMedCrossRef
27.
29.
go back to reference Saraswathy S (2006) Semi-automated segmentation of brain tumor lesions in MR images [abstract]. International Society of Magnetic Resonance Imaging, Seattle Saraswathy S (2006) Semi-automated segmentation of brain tumor lesions in MR images [abstract]. International Society of Magnetic Resonance Imaging, Seattle
30.
go back to reference Zhang Y, Brady M, Smith S (2001) Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging 20:45–57. doi:10.1109/42.906424 PubMedCrossRef Zhang Y, Brady M, Smith S (2001) Segmentation of brain MR images through a hidden Markov random field model and the expectation-maximization algorithm. IEEE Trans Med Imaging 20:45–57. doi:10.​1109/​42.​906424 PubMedCrossRef
31.
go back to reference Chan AA, Nelson SJ (2004) Simplified gamma-variate fitting of perfusion curves. In: Biomedical imaging: macro to nano. IEEE international symposium, vol 2, pp 1067–1070 Chan AA, Nelson SJ (2004) Simplified gamma-variate fitting of perfusion curves. In: Biomedical imaging: macro to nano. IEEE international symposium, vol 2, pp 1067–1070
32.
go back to reference Johnson G, Wetzel SG, Cha S, Babb J, Tofts PS (2004) Measuring blood volume and vascular transfer constant from dynamic, T(2)*-weighted contrast-enhanced MRI. Magn Reson Med 51:961–968. doi:10.1002/mrm.20049 PubMedCrossRef Johnson G, Wetzel SG, Cha S, Babb J, Tofts PS (2004) Measuring blood volume and vascular transfer constant from dynamic, T(2)*-weighted contrast-enhanced MRI. Magn Reson Med 51:961–968. doi:10.​1002/​mrm.​20049 PubMedCrossRef
33.
go back to reference Lee MC, Cha S, Chang SM, Nelson SJ (2005) Dynamic susceptibility contrast perfusion imaging of radiation effects in normal-appearing brain tissue: changes in the first-pass and recirculation phases. J Magn Reson Imaging 21:683–693. doi:10.1002/jmri.20298 PubMedCrossRef Lee MC, Cha S, Chang SM, Nelson SJ (2005) Dynamic susceptibility contrast perfusion imaging of radiation effects in normal-appearing brain tissue: changes in the first-pass and recirculation phases. J Magn Reson Imaging 21:683–693. doi:10.​1002/​jmri.​20298 PubMedCrossRef
34.
go back to reference Hartkens T, Rueckert D, Schnabel JA, Hawkes DJ, Hill DLG (2002) VTK CISG registration toolkit: an open source software package for affine and non-rigid registration of single- and multimodal 3D images. [abstract] BVM 2002. Springer-Verlag, Leipzig Hartkens T, Rueckert D, Schnabel JA, Hawkes DJ, Hill DLG (2002) VTK CISG registration toolkit: an open source software package for affine and non-rigid registration of single- and multimodal 3D images. [abstract] BVM 2002. Springer-Verlag, Leipzig
35.
go back to reference Moonen CT, von Kienlin M, van Zijl PC, Cohen J, Gillen J, Daly P et al (1989) Comparison of single-shot localization methods (STEAM and PRESS) for in vivo proton NMR spectroscopy. NMR Biomed 2:201–208. doi:10.1002/nbm.1940020506 PubMedCrossRef Moonen CT, von Kienlin M, van Zijl PC, Cohen J, Gillen J, Daly P et al (1989) Comparison of single-shot localization methods (STEAM and PRESS) for in vivo proton NMR spectroscopy. NMR Biomed 2:201–208. doi:10.​1002/​nbm.​1940020506 PubMedCrossRef
36.
go back to reference Tran TK, Vigneron DB, Sailasuta N, Tropp J, Le Roux P, Kurhanewicz J et al (2000) Very selective suppression pulses for clinical MRSI studies of brain and prostate cancer. Magn Reson Med 43:23–33. doi:10.1002/(SICI)1522-2594(200001)43:1<23::AID-MRM4>3.0.CO;2-EPubMedCrossRef Tran TK, Vigneron DB, Sailasuta N, Tropp J, Le Roux P, Kurhanewicz J et al (2000) Very selective suppression pulses for clinical MRSI studies of brain and prostate cancer. Magn Reson Med 43:23–33. doi:10.1002/(SICI)1522-2594(200001)43:1<23::AID-MRM4>3.0.CO;2-EPubMedCrossRef
37.
go back to reference Star-Lack J, Spielman D, Adalsteinsson E, Kurhanewicz J, Terris DJ, Vigneron DB (1998) In vivo lactate editing with simultaneous detection of choline, creatine, NAA, and lipid singlets at 1.5 T using PRESS excitation with applications to the study of brain and head and neck tumors. J Magn Reson 133:243–254. doi:10.1006/jmre.1998.1458 PubMedCrossRef Star-Lack J, Spielman D, Adalsteinsson E, Kurhanewicz J, Terris DJ, Vigneron DB (1998) In vivo lactate editing with simultaneous detection of choline, creatine, NAA, and lipid singlets at 1.5 T using PRESS excitation with applications to the study of brain and head and neck tumors. J Magn Reson 133:243–254. doi:10.​1006/​jmre.​1998.​1458 PubMedCrossRef
40.
go back to reference McKnight TR, Noworolski SM, Vigneron DB, Nelson SJ (2001) An automated technique for the quantitative assessment of 3D-MRSI data from patients with glioma. J Magn Reson Imaging 13:167–177. doi:10.1002/1522-2586(200102)13:2<167::AID-JMRI1026>3.0.CO;2-KPubMedCrossRef McKnight TR, Noworolski SM, Vigneron DB, Nelson SJ (2001) An automated technique for the quantitative assessment of 3D-MRSI data from patients with glioma. J Magn Reson Imaging 13:167–177. doi:10.1002/1522-2586(200102)13:2<167::AID-JMRI1026>3.0.CO;2-KPubMedCrossRef
41.
go back to reference Catalaa I, Henry R, Dillon WP, Graves EE, McKnight TR, Lu Y et al (2006) Perfusion, diffusion and spectroscopy values in newly diagnosed cerebral gliomas. NMR Biomed 19:463–475. doi:10.1002/nbm.1059 PubMedCrossRef Catalaa I, Henry R, Dillon WP, Graves EE, McKnight TR, Lu Y et al (2006) Perfusion, diffusion and spectroscopy values in newly diagnosed cerebral gliomas. NMR Biomed 19:463–475. doi:10.​1002/​nbm.​1059 PubMedCrossRef
42.
go back to reference Law M, Yang S, Wang H, Babb JS, Johnson G, Cha S et al (2003) Glioma grading: sensitivity, specificity, and predictive values of perfusion MR imaging and proton MR spectroscopic imaging compared with conventional MR imaging. AJNR Am J Neuroradiol 24:1989–1998PubMed Law M, Yang S, Wang H, Babb JS, Johnson G, Cha S et al (2003) Glioma grading: sensitivity, specificity, and predictive values of perfusion MR imaging and proton MR spectroscopic imaging compared with conventional MR imaging. AJNR Am J Neuroradiol 24:1989–1998PubMed
43.
go back to reference Lupo JM, Cha S, Chang SM, Nelson SJ (2005) Dynamic susceptibility-weighted perfusion imaging of high-grade gliomas: characterization of spatial heterogeneity. AJNR Am J Neuroradiol 26:1446–1454PubMed Lupo JM, Cha S, Chang SM, Nelson SJ (2005) Dynamic susceptibility-weighted perfusion imaging of high-grade gliomas: characterization of spatial heterogeneity. AJNR Am J Neuroradiol 26:1446–1454PubMed
44.
go back to reference Cha S, Lupo JM, Chen MH, Lamborn KR, McDermott MW, Berger MS et al (2007) Differentiation of glioblastoma multiforme and single brain metastasis by peak height and percentage of signal intensity recovery derived from dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging. AJNR Am J Neuroradiol 28:1078–1084. doi:10.3174/ajnr.A0484 PubMedCrossRef Cha S, Lupo JM, Chen MH, Lamborn KR, McDermott MW, Berger MS et al (2007) Differentiation of glioblastoma multiforme and single brain metastasis by peak height and percentage of signal intensity recovery derived from dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging. AJNR Am J Neuroradiol 28:1078–1084. doi:10.​3174/​ajnr.​A0484 PubMedCrossRef
45.
go back to reference Lupo JM, Lee MC, Han ET, Cha S, Chang SM, Berger MS et al (2006) Feasibility of dynamic susceptibility contrast perfusion MR imaging at 3T using a standard quadrature head coil and eight-channel phased-array coil with and without SENSE reconstruction. J Magn Reson Imaging 24:520–529. doi:10.1002/jmri.20673 PubMedCrossRef Lupo JM, Lee MC, Han ET, Cha S, Chang SM, Berger MS et al (2006) Feasibility of dynamic susceptibility contrast perfusion MR imaging at 3T using a standard quadrature head coil and eight-channel phased-array coil with and without SENSE reconstruction. J Magn Reson Imaging 24:520–529. doi:10.​1002/​jmri.​20673 PubMedCrossRef
46.
go back to reference Rana AK, Wardlaw JM, Armitage PA, Bastin ME (2003) Apparent diffusion coefficient (ADC) measurements may be more reliable and reproducible than lesion volume on diffusion-weighted images from patients with acute ischaemic stroke-implications for study design. Magn Reson Imaging 21:617–624. doi:10.1016/S0730-725X(03)00087-0 PubMedCrossRef Rana AK, Wardlaw JM, Armitage PA, Bastin ME (2003) Apparent diffusion coefficient (ADC) measurements may be more reliable and reproducible than lesion volume on diffusion-weighted images from patients with acute ischaemic stroke-implications for study design. Magn Reson Imaging 21:617–624. doi:10.​1016/​S0730-725X(03)00087-0 PubMedCrossRef
47.
go back to reference Sinha S, Bastin ME, Whittle IR, Wardlaw JM (2002) Diffusion tensor MR imaging of high-grade cerebral gliomas. AJNR Am J Neuroradiol 23:520–527PubMed Sinha S, Bastin ME, Whittle IR, Wardlaw JM (2002) Diffusion tensor MR imaging of high-grade cerebral gliomas. AJNR Am J Neuroradiol 23:520–527PubMed
48.
go back to reference Henkelman RM (1990) Diffusion-weighted MR imaging: a useful adjunct to clinical diagnosis or a scientific curiosity? AJNR Am J Neuroradiol 11:932–934 Henkelman RM (1990) Diffusion-weighted MR imaging: a useful adjunct to clinical diagnosis or a scientific curiosity? AJNR Am J Neuroradiol 11:932–934
50.
go back to reference Tien RD, Felsberg GJ, Friedman H, Brown M, MacFall J (1994) MR imaging of high-grade cerebral gliomas: value of diffusion-weighted echoplanar pulse sequences. AJR Am J Roentgenol 162:671–677PubMed Tien RD, Felsberg GJ, Friedman H, Brown M, MacFall J (1994) MR imaging of high-grade cerebral gliomas: value of diffusion-weighted echoplanar pulse sequences. AJR Am J Roentgenol 162:671–677PubMed
51.
go back to reference Gauvain KM, McKinstry RC, Mukherjee P, Perry A, Neil JJ, Kaufman BA et al (2001) Evaluating pediatric brain tumor cellularity with diffusion-tensor imaging. AJR Am J Roentgenol 177:449–454PubMed Gauvain KM, McKinstry RC, Mukherjee P, Perry A, Neil JJ, Kaufman BA et al (2001) Evaluating pediatric brain tumor cellularity with diffusion-tensor imaging. AJR Am J Roentgenol 177:449–454PubMed
53.
go back to reference Ozturk E, Banerjee S, Majumdar S, Nelson SJ (2006) Partially parallel MR spectroscopic imaging of gliomas at 3T. Conf Proc IEEE Eng Med Biol Soc 1:493–496PubMed Ozturk E, Banerjee S, Majumdar S, Nelson SJ (2006) Partially parallel MR spectroscopic imaging of gliomas at 3T. Conf Proc IEEE Eng Med Biol Soc 1:493–496PubMed
Metadata
Title
Relationship of pre-surgery metabolic and physiological MR imaging parameters to survival for patients with untreated GBM
Authors
Forrest W. Crawford
Inas S. Khayal
Colleen McGue
Suja Saraswathy
Andrea Pirzkall
Soonmee Cha
Kathleen R. Lamborn
Susan M. Chang
Mitchel S. Berger
Sarah J. Nelson
Publication date
01-02-2009
Publisher
Springer US
Published in
Journal of Neuro-Oncology / Issue 3/2009
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI
https://doi.org/10.1007/s11060-008-9719-x

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