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Published in: Journal of Neuro-Oncology 2/2016

01-01-2016 | Clinical Study

Advanced MRI may complement histological diagnosis of lower grade gliomas and help in predicting survival

Authors: Valeria Cuccarini, A. Erbetta, M. Farinotti, L. Cuppini, F. Ghielmetti, B. Pollo, F. Di Meco, M. Grisoli, G. Filippini, G. Finocchiaro, M. G. Bruzzone, M. Eoli

Published in: Journal of Neuro-Oncology | Issue 2/2016

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Abstract

MRI grading of grade II and III gliomas may have an important impact on treatment decisions. Occasionally, both conventional MRI (cMRI) and histology fail to clearly establish the tumour grade. Three cMRI features (no necrosis; no relevant oedema; absent or faint contrast enhancement) previously validated in 196 patients with supratentorial gliomas directed our selection of 68 suspected low-grade gliomas (LGG) that were also investigated by advanced MRI (aMRI), including perfusion weighted imaging (PWI), diffusion weighted imaging (DWI) and spectroscopy. All the gliomas had histopathological diagnoses. Sensitivity and specificity of cMRI pre-operative diagnosis were 78.5 and 38.5 %, respectively, and 85.7 and 53.8 % when aMRI was included, respectively. ROC analysis showed that cut-off values of 1.29 for maximum rCBV, 1.69 for minimum rADC, 2.1 for rCho/Cr ratio could differentiate between LGG and HGG with a sensitivity of 61.5, 53.8, and 53.8 % and a specificity of 54.7, 43 and 64.3 %, respectively. A significantly longer OS was observed in patients with a maximum rCBV <1.46 and minimum rADC >1.69 (80 vs 55 months, p = 0.01; 80 vs 51 months, p = 0.002, respectively). This result was also confirmed when cases were stratified according to pathology (LGG vs HGG). The ability of aMRI to differentiate between LGG and HGG and to predict survival improved as the number of aMRI techniques considered increased. In a selected population of suspected LGG, classification by cMRI underestimated the actual fraction of HGG. aMRI slightly increased the diagnostic accuracy compared to histopathology. However, DWI and PWI were prognostic markers independent of histological grade.
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Literature
2.
go back to reference Lang FF, Gilbert MR (2006) Diffusely infiltrative low-grade gliomas in adults. J Clin Oncol 24:1236–1245PubMedCrossRef Lang FF, Gilbert MR (2006) Diffusely infiltrative low-grade gliomas in adults. J Clin Oncol 24:1236–1245PubMedCrossRef
3.
go back to reference Bulakbasi N, Guvenc I, Onguru O, Erdogan E, Tayfun C, Ucoz T (2004) The added value of the apparent diffusion coefficient calculation to magnetic resonance imaging in the differentiation and grading of malignant brain tumors. J Comput Assist Tomogr 28:735–746PubMedCrossRef Bulakbasi N, Guvenc I, Onguru O, Erdogan E, Tayfun C, Ucoz T (2004) The added value of the apparent diffusion coefficient calculation to magnetic resonance imaging in the differentiation and grading of malignant brain tumors. J Comput Assist Tomogr 28:735–746PubMedCrossRef
4.
go back to reference Law M, Yang S, Wang H, Babb JS, Johnson G, Cha S, Knopp EA, Zagzag D (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, Knopp EA, Zagzag D (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
5.
go back to reference Pallud J, Capelle L, Taillandier L et al (2009) Prognostic significance of imaging contrast enhancement for WHO grade II gliomas. Neuro Oncol 11:176–182PubMedPubMedCentralCrossRef Pallud J, Capelle L, Taillandier L et al (2009) Prognostic significance of imaging contrast enhancement for WHO grade II gliomas. Neuro Oncol 11:176–182PubMedPubMedCentralCrossRef
6.
go back to reference Scarabino T, Popolizio T, Trojsi F, Giannatempo G, Pollice S, Maggialetti N, Carriero A, Di Costanzo A, Tedeschi G, Salvolini U (2009) Role of advanced MR imaging modalities in diagnosing cerebral gliomas. Radiol Med 114:448–460PubMedCrossRef Scarabino T, Popolizio T, Trojsi F, Giannatempo G, Pollice S, Maggialetti N, Carriero A, Di Costanzo A, Tedeschi G, Salvolini U (2009) Role of advanced MR imaging modalities in diagnosing cerebral gliomas. Radiol Med 114:448–460PubMedCrossRef
7.
go back to reference Kim JH, Chang KH, Na DG, Song IC, Kwon BJ, Han MH, Kim K (2006) 3T 1H-MR spectroscopy in grading of cerebral gliomas: comparison of short and intermediate echo time sequences. Am J Neuroradiol 27:1412–1418PubMed Kim JH, Chang KH, Na DG, Song IC, Kwon BJ, Han MH, Kim K (2006) 3T 1H-MR spectroscopy in grading of cerebral gliomas: comparison of short and intermediate echo time sequences. Am J Neuroradiol 27:1412–1418PubMed
8.
go back to reference Weber M-A, Giesel FL, Stieltjes B (2008) MRI for identification of progression in brain tumors: from morphology to function. Expert Rev Neurother 8:1507–1525PubMedCrossRef Weber M-A, Giesel FL, Stieltjes B (2008) MRI for identification of progression in brain tumors: from morphology to function. Expert Rev Neurother 8:1507–1525PubMedCrossRef
9.
go back to reference Fan GG, Deng QL, Wu ZH, Guo QY (2006) Usefulness of diffusion/perfusion-weighted MRI in patients with non-enhancing supratentorial brain gliomas: a valuable tool to predict tumour grading? Br J Radiol 79:652–658PubMedCrossRef Fan GG, Deng QL, Wu ZH, Guo QY (2006) Usefulness of diffusion/perfusion-weighted MRI in patients with non-enhancing supratentorial brain gliomas: a valuable tool to predict tumour grading? Br J Radiol 79:652–658PubMedCrossRef
10.
go back to reference Chaskis C, Stadnik T, Michotte A, Van Rompaey K, D’Haens J (2006) Prognostic value of perfusion-weighted imaging in brain glioma: a prospective study. Acta Neurochir (Wien) 148:277–285CrossRef Chaskis C, Stadnik T, Michotte A, Van Rompaey K, D’Haens J (2006) Prognostic value of perfusion-weighted imaging in brain glioma: a prospective study. Acta Neurochir (Wien) 148:277–285CrossRef
11.
go back to reference Arvinda HR, Kesavadas C, Sarma PS, Thomas B, Radhakrishnan VV, Gupta AK, Kapilamoorthy TR, Nair S (2009) Glioma grading: sensitivity, specificity, positive and negative predictive values of diffusion and perfusion imaging. J Neurooncol 94:87–96PubMedCrossRef Arvinda HR, Kesavadas C, Sarma PS, Thomas B, Radhakrishnan VV, Gupta AK, Kapilamoorthy TR, Nair S (2009) Glioma grading: sensitivity, specificity, positive and negative predictive values of diffusion and perfusion imaging. J Neurooncol 94:87–96PubMedCrossRef
12.
go back to reference McKnight TR, Lamborn KR, Love TD, Berger MS, Chang S, Dillon WP, Bollen A, Nelson SJ (2007) Correlation of magnetic resonance spectroscopic and growth characteristics within Grades II and III gliomas. J Neurosurg 106:660–666PubMedCrossRef McKnight TR, Lamborn KR, Love TD, Berger MS, Chang S, Dillon WP, Bollen A, Nelson SJ (2007) Correlation of magnetic resonance spectroscopic and growth characteristics within Grades II and III gliomas. J Neurosurg 106:660–666PubMedCrossRef
13.
go back to reference Chang SM, Nelson S, Vandenberg S et al (2009) Integration of preoperative anatomic and metabolic physiologic imaging of newly diagnosed glioma. J Neurooncol 92:401–415PubMedPubMedCentralCrossRef Chang SM, Nelson S, Vandenberg S et al (2009) Integration of preoperative anatomic and metabolic physiologic imaging of newly diagnosed glioma. J Neurooncol 92:401–415PubMedPubMedCentralCrossRef
14.
go back to reference Sugahara T, Korogi Y, Kochi M et al (1999) Usefulness of diffusion-weighted MRI with echo-planar technique in the evaluation of cellularity in gliomas. J Magn Reson Imaging 9:53–60PubMedCrossRef Sugahara T, Korogi Y, Kochi M et al (1999) Usefulness of diffusion-weighted MRI with echo-planar technique in the evaluation of cellularity in gliomas. J Magn Reson Imaging 9:53–60PubMedCrossRef
15.
go back to reference Gerstner ER, Sorensen AG, Jain RK, Batchelor TT (2008) Advances in neuroimaging techniques for the evaluation of tumor growth, vascular permeability, and angiogenesis in gliomas. Curr Opin Neurol 21:728–735PubMedCrossRef Gerstner ER, Sorensen AG, Jain RK, Batchelor TT (2008) Advances in neuroimaging techniques for the evaluation of tumor growth, vascular permeability, and angiogenesis in gliomas. Curr Opin Neurol 21:728–735PubMedCrossRef
16.
go back to reference Weber MA, Zoubaa S, Schlieter M et al (2006) Diagnostic performance of spectroscopic and perfusion MRI for distinction of brain tumors. Neurology 66:1899–1906PubMedCrossRef Weber MA, Zoubaa S, Schlieter M et al (2006) Diagnostic performance of spectroscopic and perfusion MRI for distinction of brain tumors. Neurology 66:1899–1906PubMedCrossRef
17.
go back to reference Xu V, Chan H, Lin AP, Sailasuta N, Valencerina S, Tran T, Hovener J, Ross BD (2008) MR spectroscopy in diagnosis and neurological decision-making. Semin Neurol 28:407–422PubMedCrossRef Xu V, Chan H, Lin AP, Sailasuta N, Valencerina S, Tran T, Hovener J, Ross BD (2008) MR spectroscopy in diagnosis and neurological decision-making. Semin Neurol 28:407–422PubMedCrossRef
18.
go back to reference Lam WWM, Poon WS, Metreweli C (2002) Diffusion MR imaging in glioma: does it have any role in the pre-operation determination of grading of glioma? Clin Radiol 57:219–225PubMedCrossRef Lam WWM, Poon WS, Metreweli C (2002) Diffusion MR imaging in glioma: does it have any role in the pre-operation determination of grading of glioma? Clin Radiol 57:219–225PubMedCrossRef
19.
go back to reference Al-Okaili RN, Krejza J, Wang S, Woo JH, Melhem ER (2006) Advanced MR imaging techniques in the diagnosis of intraaxial brain tumors in adults. Radiographics 26(Suppl 1):S173–S189PubMedCrossRef Al-Okaili RN, Krejza J, Wang S, Woo JH, Melhem ER (2006) Advanced MR imaging techniques in the diagnosis of intraaxial brain tumors in adults. Radiographics 26(Suppl 1):S173–S189PubMedCrossRef
20.
go back to reference Hlaihel C, Guilloton L, Guyotat J, Streichenberger N, Honnorat J, Cotton F (2010) Predictive value of multimodality MRI using conventional, perfusion, and spectroscopy MR in anaplastic transformation of low-grade oligodendrogliomas. J Neurooncol 97:73–80PubMedCrossRef Hlaihel C, Guilloton L, Guyotat J, Streichenberger N, Honnorat J, Cotton F (2010) Predictive value of multimodality MRI using conventional, perfusion, and spectroscopy MR in anaplastic transformation of low-grade oligodendrogliomas. J Neurooncol 97:73–80PubMedCrossRef
21.
go back to reference Morita N, Wang S, Chawla S, Poptani H, Melhem ER (2010) Dynamic susceptibility contrast perfusion weighted imaging in grading of nonenhancing astrocytomas. J Magn Reson Imaging 32:803–808PubMedCrossRef Morita N, Wang S, Chawla S, Poptani H, Melhem ER (2010) Dynamic susceptibility contrast perfusion weighted imaging in grading of nonenhancing astrocytomas. J Magn Reson Imaging 32:803–808PubMedCrossRef
22.
go back to reference Server A, Kulle B, Gadmar ØB, Josefsen R, Kumar T, Nakstad PH (2011) Measurements of diagnostic examination performance using quantitative apparent diffusion coefficient and proton MR spectroscopic imaging in the preoperative evaluation of tumor grade in cerebral gliomas. Eur J Radiol 80:462–470PubMedCrossRef Server A, Kulle B, Gadmar ØB, Josefsen R, Kumar T, Nakstad PH (2011) Measurements of diagnostic examination performance using quantitative apparent diffusion coefficient and proton MR spectroscopic imaging in the preoperative evaluation of tumor grade in cerebral gliomas. Eur J Radiol 80:462–470PubMedCrossRef
23.
go back to reference Murakami R, Hirai T, Sugahara T et al (2009) Grading astrocytic tumors by using apparent diffusion coefficient parameters: superiority of a one- versus two-parameter pilot method. Radiology 251:838–845PubMedCrossRef Murakami R, Hirai T, Sugahara T et al (2009) Grading astrocytic tumors by using apparent diffusion coefficient parameters: superiority of a one- versus two-parameter pilot method. Radiology 251:838–845PubMedCrossRef
24.
go back to reference Khalid L, Carone M, Dumrongpisutikul N, Intrapiromkul J, Bonekamp D, Barker PB, Yousem DM (2012) Imaging characteristics of oligodendrogliomas that predict grade. Am J Neuroradiol 33:852–857PubMedPubMedCentralCrossRef Khalid L, Carone M, Dumrongpisutikul N, Intrapiromkul J, Bonekamp D, Barker PB, Yousem DM (2012) Imaging characteristics of oligodendrogliomas that predict grade. Am J Neuroradiol 33:852–857PubMedPubMedCentralCrossRef
25.
go back to reference Sahin N, Melhem ER, Wang S, Krejza J, Poptani H, Chawla S, Verma G (2013) Advanced MR imaging techniques in the evaluation of nonenhancing gliomas: perfusion-weighted imaging compared with proton magnetic resonance spectroscopy and tumor grade. Neuroradiol J 26:531–541PubMedCrossRef Sahin N, Melhem ER, Wang S, Krejza J, Poptani H, Chawla S, Verma G (2013) Advanced MR imaging techniques in the evaluation of nonenhancing gliomas: perfusion-weighted imaging compared with proton magnetic resonance spectroscopy and tumor grade. Neuroradiol J 26:531–541PubMedCrossRef
26.
go back to reference Liu Z, Zhou Q, Zeng Q, Li C-F, Zhang K (2012) Noninvasive evaluation of cerebral glioma grade by using diffusion-weighted imaging-guided single-voxel proton magnetic resonance spectroscopy. J Int Med Res 40:76–84PubMedCrossRef Liu Z, Zhou Q, Zeng Q, Li C-F, Zhang K (2012) Noninvasive evaluation of cerebral glioma grade by using diffusion-weighted imaging-guided single-voxel proton magnetic resonance spectroscopy. J Int Med Res 40:76–84PubMedCrossRef
27.
go back to reference Law M, Young RJ, Babb JS, Peccerelli N, Chheang S, Gruber ML, Miller DC, Golfinos JG (2008) Gliomas: predicting time to progression or survival with cerebral blood volume measurements at dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging. Radiology 2:490–498CrossRef Law M, Young RJ, Babb JS, Peccerelli N, Chheang S, Gruber ML, Miller DC, Golfinos JG (2008) Gliomas: predicting time to progression or survival with cerebral blood volume measurements at dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging. Radiology 2:490–498CrossRef
28.
go back to reference Maia ACM, Malheiros SMF, da Rocha AJ, da Silva CJ, Gabbai AA, Ferraz FAP, Stávale JN (2005) MR cerebral blood volume maps correlated with vascular endothelial growth factor expression and tumor grade in nonenhancing gliomas. AJNR Am J Neuroradiol 26:777–783PubMed Maia ACM, Malheiros SMF, da Rocha AJ, da Silva CJ, Gabbai AA, Ferraz FAP, Stávale JN (2005) MR cerebral blood volume maps correlated with vascular endothelial growth factor expression and tumor grade in nonenhancing gliomas. AJNR Am J Neuroradiol 26:777–783PubMed
29.
go back to reference Cui Y, Ma L, Chen X, Zhang Z, Jiang H, Lin S (2014) Lower apparent diffusion coefficients indicate distinct prognosis in low-grade and high-grade glioma. J Neurooncol 119:377–385PubMedCrossRef Cui Y, Ma L, Chen X, Zhang Z, Jiang H, Lin S (2014) Lower apparent diffusion coefficients indicate distinct prognosis in low-grade and high-grade glioma. J Neurooncol 119:377–385PubMedCrossRef
30.
go back to reference Zulfiqar M, Yousem DM, Lai H (2013) ADC values and prognosis of malignant astrocytomas: does lower ADC predict a worse prognosis independent of grade of tumor?-a meta-analysis. Am J Roentgenol 200:624–629CrossRef Zulfiqar M, Yousem DM, Lai H (2013) ADC values and prognosis of malignant astrocytomas: does lower ADC predict a worse prognosis independent of grade of tumor?-a meta-analysis. Am J Roentgenol 200:624–629CrossRef
31.
go back to reference Caseiras GB, Chheang S, Babb J et al (2010) Relative cerebral blood volume measurements of low-grade gliomas predict patient outcome in a multi-institution setting. Eur J Radiol 73:215–220PubMedCrossRef Caseiras GB, Chheang S, Babb J et al (2010) Relative cerebral blood volume measurements of low-grade gliomas predict patient outcome in a multi-institution setting. Eur J Radiol 73:215–220PubMedCrossRef
32.
go back to reference Bisdas S, Kirkpatrick M, Giglio P, Welsh C, Spampinato MV, Rumboldt Z (2009) Cerebral blood volume measurements by perfusion-weighted MR imaging in gliomas: ready for prime time in predicting short-term outcome and recurrent disease? Am J Neuroradiol 30:681–688PubMedCrossRef Bisdas S, Kirkpatrick M, Giglio P, Welsh C, Spampinato MV, Rumboldt Z (2009) Cerebral blood volume measurements by perfusion-weighted MR imaging in gliomas: ready for prime time in predicting short-term outcome and recurrent disease? Am J Neuroradiol 30:681–688PubMedCrossRef
33.
go back to reference Majchrzak K, Kaspera W, Bobek-Billewicz B, Hebda A, Stasik-Pres G, Majchrzak H, Ladzinski P (2012) The assessment of prognostic factors in surgical treatment of low-grade gliomas: a prospective study. Clin Neurol Neurosurg 114:1135–1144PubMedCrossRef Majchrzak K, Kaspera W, Bobek-Billewicz B, Hebda A, Stasik-Pres G, Majchrzak H, Ladzinski P (2012) The assessment of prognostic factors in surgical treatment of low-grade gliomas: a prospective study. Clin Neurol Neurosurg 114:1135–1144PubMedCrossRef
34.
go back to reference Hattingen E, Delic O, Franz K, Pilatus U, Raab P, Lanfermann H, Gerlach R (2010) (1)H MRSI and progression-free survival in patients with WHO grades II and III gliomas. Neurol Res 32:593–602PubMedCrossRef Hattingen E, Delic O, Franz K, Pilatus U, Raab P, Lanfermann H, Gerlach R (2010) (1)H MRSI and progression-free survival in patients with WHO grades II and III gliomas. Neurol Res 32:593–602PubMedCrossRef
35.
go back to reference Lober RM, Cho YJ, Tang Y, Barnes PD, Edwards MS, Vogel H, Fisher PG, Monje M, Yeom KW (2014) Diffusion-weighted MRI derived apparent diffusion coefficient identifies prognostically distinct subgroups of pediatric diffuse intrinsic pontine glioma. J. Neurooncol. 117:175–182PubMedCrossRef Lober RM, Cho YJ, Tang Y, Barnes PD, Edwards MS, Vogel H, Fisher PG, Monje M, Yeom KW (2014) Diffusion-weighted MRI derived apparent diffusion coefficient identifies prognostically distinct subgroups of pediatric diffuse intrinsic pontine glioma. J. Neurooncol. 117:175–182PubMedCrossRef
36.
go back to reference Zonari P, Baraldi P, Crisi G (2007) Multimodal MRI in the characterization of glial neoplasms: the combined role of single-voxel MR spectroscopy, diffusion imaging and echo-planar perfusion imaging. Neuroradiology 49:795–803PubMedCrossRef Zonari P, Baraldi P, Crisi G (2007) Multimodal MRI in the characterization of glial neoplasms: the combined role of single-voxel MR spectroscopy, diffusion imaging and echo-planar perfusion imaging. Neuroradiology 49:795–803PubMedCrossRef
37.
go back to reference Senft C, Hattingen E, Pilatus U, Franz K, Schänzer A, Lanfermann H, Seifert V, Gasser T (2009) Diagnostic value of proton magnetic resonance spectroscopy in the noninvasive grading of solid gliomas: comparison of maximum and mean choline values. Neurosurgery 65:908–913PubMedCrossRef Senft C, Hattingen E, Pilatus U, Franz K, Schänzer A, Lanfermann H, Seifert V, Gasser T (2009) Diagnostic value of proton magnetic resonance spectroscopy in the noninvasive grading of solid gliomas: comparison of maximum and mean choline values. Neurosurgery 65:908–913PubMedCrossRef
38.
go back to reference Macdonald DR, Cascino TL, Schold SC Jr, Cairncross JG (1990) Response criteria for phase II studies of supratentorial malignant glioma. J Clin Oncol 8:1277–1280PubMed Macdonald DR, Cascino TL, Schold SC Jr, Cairncross JG (1990) Response criteria for phase II studies of supratentorial malignant glioma. J Clin Oncol 8:1277–1280PubMed
39.
go back to reference Van den Bent MJ, Wefel JS, Schiff D et al (2011) Response assessment in neuro-oncology (a report of the RANO group): assessment of outcome in trials of diffuse low-grade gliomas. Lancet Oncol 12:583–593PubMedCrossRef Van den Bent MJ, Wefel JS, Schiff D et al (2011) Response assessment in neuro-oncology (a report of the RANO group): assessment of outcome in trials of diffuse low-grade gliomas. Lancet Oncol 12:583–593PubMedCrossRef
40.
go back to reference Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114:97–109PubMedPubMedCentralCrossRef Louis DN, Ohgaki H, Wiestler OD, Cavenee WK, Burger PC, Jouvet A, Scheithauer BW, Kleihues P (2007) The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 114:97–109PubMedPubMedCentralCrossRef
42.
go back to reference Yoon JH, Kim JH, Kang WJ, Sohn C-HH, Choi SH, Yun TJ, Eun Y, Song YS, Chang K-HH (2014) Grading of cerebral glioma with multiparametric MR imaging and 18F-FDG-PET: concordance and accuracy. Eur Radiol 24:380–389PubMedCrossRef Yoon JH, Kim JH, Kang WJ, Sohn C-HH, Choi SH, Yun TJ, Eun Y, Song YS, Chang K-HH (2014) Grading of cerebral glioma with multiparametric MR imaging and 18F-FDG-PET: concordance and accuracy. Eur Radiol 24:380–389PubMedCrossRef
43.
go back to reference Eoli M, Menghi F, Bruzzone MG et al (2007) Methylation of O6-methylguanine DNA methyltransferase and loss of heterozygosity on 19q and/or 17p are overlapping features of secondary glioblastomas with prolonged survival. Clin Cancer Res 13:2606–2613PubMedCrossRef Eoli M, Menghi F, Bruzzone MG et al (2007) Methylation of O6-methylguanine DNA methyltransferase and loss of heterozygosity on 19q and/or 17p are overlapping features of secondary glioblastomas with prolonged survival. Clin Cancer Res 13:2606–2613PubMedCrossRef
44.
go back to reference Pallud J, Blonski M, Mandonnet E, Audureau E, Fontaine D, Sanai N, Bauchet L, Peruzzi P, Frenay M, Colin P, Guillevin R, Bernier V, Baron MH, Guyotat J, Duffau H, Taillandier L, Capelle L (2013) Velocity of tumor spontaneous expansion predicts long-term outcomes for diffuse low-grade gliomas. Neuro-oncol 15(5):595–606PubMedPubMedCentralCrossRef Pallud J, Blonski M, Mandonnet E, Audureau E, Fontaine D, Sanai N, Bauchet L, Peruzzi P, Frenay M, Colin P, Guillevin R, Bernier V, Baron MH, Guyotat J, Duffau H, Taillandier L, Capelle L (2013) Velocity of tumor spontaneous expansion predicts long-term outcomes for diffuse low-grade gliomas. Neuro-oncol 15(5):595–606PubMedPubMedCentralCrossRef
45.
go back to reference Cancer Genome Atlas Research Network (2015) Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. NEJM 372(26):2481–2498CrossRef Cancer Genome Atlas Research Network (2015) Comprehensive, integrative genomic analysis of diffuse lower-grade gliomas. NEJM 372(26):2481–2498CrossRef
46.
go back to reference Haegler K, Wiesmann M, Böhm C, Freiherr J, Schnell O, Brückmann H, Tonn JC, Linn J (2012) New similarity search based glioma grading. Neuroradiology 54:829–837PubMedCrossRef Haegler K, Wiesmann M, Böhm C, Freiherr J, Schnell O, Brückmann H, Tonn JC, Linn J (2012) New similarity search based glioma grading. Neuroradiology 54:829–837PubMedCrossRef
47.
go back to reference Bradac O, Vrana J, Jiru F, Kramar F, Netuka D, Hrabal P, Horinek D, de Lacy P, Benes V (2014) Recognition of anaplastic foci within low-grade gliomas using MR spectroscopy. Br J Neurosurg 28:631–636PubMedCrossRef Bradac O, Vrana J, Jiru F, Kramar F, Netuka D, Hrabal P, Horinek D, de Lacy P, Benes V (2014) Recognition of anaplastic foci within low-grade gliomas using MR spectroscopy. Br J Neurosurg 28:631–636PubMedCrossRef
48.
go back to reference Hilario A, Ramos A, Perez-Nuñez A, Salvador E, Millan JM, Lagares A, Sepulveda JM, Gonzalez-Leon P, Hernandez-Lain A, Ricoy JR (2012) The added value of apparent diffusion coefficient to cerebral blood volume in the preoperative grading of diffuse gliomas. Am J Neuroradiol 33:701–707PubMedCrossRef Hilario A, Ramos A, Perez-Nuñez A, Salvador E, Millan JM, Lagares A, Sepulveda JM, Gonzalez-Leon P, Hernandez-Lain A, Ricoy JR (2012) The added value of apparent diffusion coefficient to cerebral blood volume in the preoperative grading of diffuse gliomas. Am J Neuroradiol 33:701–707PubMedCrossRef
49.
go back to reference Liu X, Tian W, Kolar B, Yeaney GA, Qiu X, Johnson MD, Ekholm S (2011) MR diffusion tensor and perfusion-weighted imaging in preoperative grading of supratentorial nonenhancing gliomas. Neuro Oncol 13:447–455PubMedPubMedCentralCrossRef Liu X, Tian W, Kolar B, Yeaney GA, Qiu X, Johnson MD, Ekholm S (2011) MR diffusion tensor and perfusion-weighted imaging in preoperative grading of supratentorial nonenhancing gliomas. Neuro Oncol 13:447–455PubMedPubMedCentralCrossRef
50.
go back to reference Cha S, Tihan T, Crawford F, Fischbein NJ, Chang S, Bollen A, Nelson SJ, Prados M, Berger MS, Dillon WP (2005) Differentiation of low-grade oligodendrogliomas from low-grade astrocytomas by using quantitative blood-volume measurements derived from dynamic susceptibility contrast-enhanced MR imaging. Am J Neuroradiol 26:266–273PubMed Cha S, Tihan T, Crawford F, Fischbein NJ, Chang S, Bollen A, Nelson SJ, Prados M, Berger MS, Dillon WP (2005) Differentiation of low-grade oligodendrogliomas from low-grade astrocytomas by using quantitative blood-volume measurements derived from dynamic susceptibility contrast-enhanced MR imaging. Am J Neuroradiol 26:266–273PubMed
Metadata
Title
Advanced MRI may complement histological diagnosis of lower grade gliomas and help in predicting survival
Authors
Valeria Cuccarini
A. Erbetta
M. Farinotti
L. Cuppini
F. Ghielmetti
B. Pollo
F. Di Meco
M. Grisoli
G. Filippini
G. Finocchiaro
M. G. Bruzzone
M. Eoli
Publication date
01-01-2016
Publisher
Springer US
Published in
Journal of Neuro-Oncology / Issue 2/2016
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI
https://doi.org/10.1007/s11060-015-1960-5

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