Skip to main content
Top
Published in: Journal of Neuro-Oncology 2/2013

Open Access 01-09-2013 | Clinical Study

Perfusion and diffusion MRI combined with 11C-methionine PET in the preoperative evaluation of suspected adult low-grade gliomas

Authors: Shala Ghaderi Berntsson, Anna Falk, Irina Savitcheva, Andrea Godau, Maria Zetterling, Göran Hesselager, Irina Alafuzoff, Elna-Marie Larsson, Anja Smits

Published in: Journal of Neuro-Oncology | Issue 2/2013

Login to get access

Abstract

Perfusion and diffusion magnetic resonance imaging (pMRI, dMRI) are valuable diagnostic tools for assessing brain tumors in the clinical setting. The aim of this study was to determine the correlation of pMRI and dMRI with 11C-methionine positron emission tomography (MET PET) in suspected low-grade gliomas (LGG) prior to surgery. Twenty-four adults with suspected LGG were enrolled in an observational study and examined by MET PET, pMRI and dMRI. Histological tumor diagnosis was confirmed in 23/24 patients (18 gliomas grade II, 5 gliomas grade III). The maximum relative cerebral blood volume (rCBVmax) and the minimum mean diffusivity (MDmin) were measured in tumor areas with highest MET uptake (hotspot) on PET by using automated co-registration of MRI and PET scans. A clearly defined hotspot on PET was present in all 23 tumors. Regions with rCBVmax corresponded with hotspot regions in all tumors, regions with MDmin corresponded with hotspot regions in 20/23 tumors. The correlation between rCBVmax (r = 0.19, P = 0.38) and MDmin (r = −0.41, P = 0.053) with MET uptake in the hotspot was not statistically significant. Taken into account the difficulties of measuring perfusion abnormalities in non-enhancing gliomas, this study demonstrates that co-registered MET PET and pMRI facilitates the identification of regions with rCBVmax. Furthermore, the lack of a clear positive correlation between tumor metabolism in terms of MET uptake and tumor vascularity measured as rCBVmax suggests that combined pMRI/PET provides complementary baseline imaging data in these tumors.
Literature
1.
2.
go back to reference Lote K, Egeland T, Hager B, Stenwig B, Skullerud K, Berg-Johnsen J, Storm-Mathisen I, Hirschberg H (1997) Survival, prognostic factors, and therapeutic efficacy in low-grade glioma: a retrospective study in 379 patients. J Clin Oncol 15:3129–3140PubMed Lote K, Egeland T, Hager B, Stenwig B, Skullerud K, Berg-Johnsen J, Storm-Mathisen I, Hirschberg H (1997) Survival, prognostic factors, and therapeutic efficacy in low-grade glioma: a retrospective study in 379 patients. J Clin Oncol 15:3129–3140PubMed
3.
go back to reference Soffietti R, Baumert BG, Bello L, von Deimling A, Duffau H, Frenay M, Grisold W, Grant R, Graus F, Hoang-Xuan K, Klein M, Melin B, Rees J, Siegal T, Smits A, Stupp R, Wick W (2010) Guidelines on management of low-grade gliomas: report of an EFNS-EANO* task force. Eur J Neurol 17:1124–1133. doi:10.1111/j.1468-1331.2010.03151.x PubMedCrossRef Soffietti R, Baumert BG, Bello L, von Deimling A, Duffau H, Frenay M, Grisold W, Grant R, Graus F, Hoang-Xuan K, Klein M, Melin B, Rees J, Siegal T, Smits A, Stupp R, Wick W (2010) Guidelines on management of low-grade gliomas: report of an EFNS-EANO* task force. Eur J Neurol 17:1124–1133. doi:10.​1111/​j.​1468-1331.​2010.​03151.​x PubMedCrossRef
4.
go back to reference Mandonnet E, Delattre JY, Tanguy ML, Swanson KR, Carpentier AF, Duffau H, Cornu P, Van Effenterre R, Alvord EC Jr, Capelle L (2003) Continuous growth of mean tumor diameter in a subset of grade II gliomas. Ann Neurol 53:524–528. doi:10.1002/ana.10528 PubMedCrossRef Mandonnet E, Delattre JY, Tanguy ML, Swanson KR, Carpentier AF, Duffau H, Cornu P, Van Effenterre R, Alvord EC Jr, Capelle L (2003) Continuous growth of mean tumor diameter in a subset of grade II gliomas. Ann Neurol 53:524–528. doi:10.​1002/​ana.​10528 PubMedCrossRef
5.
go back to reference Pallud J, Fontaine D, Duffau H, Mandonnet E, Sanai N, Taillandier L, Peruzzi P, Guillevin R, Bauchet L, Bernier V, Baron MH, Guyotat J, Capelle L (2010) Natural history of incidental World Health Organization grade II gliomas. Ann Neurol 68:727–733. doi:10.1002/ana.22106 PubMedCrossRef Pallud J, Fontaine D, Duffau H, Mandonnet E, Sanai N, Taillandier L, Peruzzi P, Guillevin R, Bauchet L, Bernier V, Baron MH, Guyotat J, Capelle L (2010) Natural history of incidental World Health Organization grade II gliomas. Ann Neurol 68:727–733. doi:10.​1002/​ana.​22106 PubMedCrossRef
7.
go back to reference Pignatti F, van den Bent M, Curran D, Debruyne C, Sylvester R, Therasse P, Afra D, Cornu P, Bolla M, Vecht C, Karim AB (2002) Prognostic factors for survival in adult patients with cerebral low-grade glioma. J Clin Oncol 20:2076–2084PubMedCrossRef Pignatti F, van den Bent M, Curran D, Debruyne C, Sylvester R, Therasse P, Afra D, Cornu P, Bolla M, Vecht C, Karim AB (2002) Prognostic factors for survival in adult patients with cerebral low-grade glioma. J Clin Oncol 20:2076–2084PubMedCrossRef
8.
go back to reference Pallud J, Taillandier L, Capelle L, Fontaine D, Peyre M, Ducray F, Duffau H, Mandonnet E (2012) Quantitative morphological magnetic resonance imaging follow-up of low-grade glioma: a plea for systematic measurement of growth rates. Neurosurgery 71:729–739. doi:10.1227/NEU.0b013e31826213de discussion 739–740PubMedCrossRef Pallud J, Taillandier L, Capelle L, Fontaine D, Peyre M, Ducray F, Duffau H, Mandonnet E (2012) Quantitative morphological magnetic resonance imaging follow-up of low-grade glioma: a plea for systematic measurement of growth rates. Neurosurgery 71:729–739. doi:10.​1227/​NEU.​0b013e31826213de​ discussion 739–740PubMedCrossRef
9.
go back to reference Aronen HJ, Gazit IE, Louis DN, Buchbinder BR, Pardo FS, Weisskoff RM, Harsh GR, Cosgrove GR, Halpern EF, Hochberg FH et al (1994) Cerebral blood volume maps of gliomas: comparison with tumor grade and histologic findings. Radiology 191:41–51PubMed Aronen HJ, Gazit IE, Louis DN, Buchbinder BR, Pardo FS, Weisskoff RM, Harsh GR, Cosgrove GR, Halpern EF, Hochberg FH et al (1994) Cerebral blood volume maps of gliomas: comparison with tumor grade and histologic findings. Radiology 191:41–51PubMed
10.
go back to reference Kono K, Inoue Y, Nakayama K, Shakudo M, Morino M, Ohata K, Wakasa K, Yamada R (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, Wakasa K, Yamada R (2001) The role of diffusion-weighted imaging in patients with brain tumors. AJNR Am J Neuroradiol 22:1081–1088PubMed
11.
go back to reference Sugahara T, Korogi Y, Kochi M, Ikushima I, Shigematu Y, Hirai T, Okuda T, Liang L, Ge Y, Komohara Y, Ushio Y, Takahashi M (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 PubMedCrossRef Sugahara T, Korogi Y, Kochi M, Ikushima I, Shigematu Y, Hirai T, Okuda T, Liang L, Ge Y, Komohara Y, Ushio Y, Takahashi M (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 PubMedCrossRef
17.
go back to reference Ericson K, Lilja A, Bergstrom M, Collins VP, Eriksson L, Ehrin E, von Holst H, Lundqvist H, Langsrom BB, Mosskin M (1985) Positron emission tomography with ([11C]methyl)-l-methionine, [11C]d-glucose, and [68 Ga]EDTA in supratentorial tumors. J Comput Assist Tomogr 9:683–689PubMedCrossRef Ericson K, Lilja A, Bergstrom M, Collins VP, Eriksson L, Ehrin E, von Holst H, Lundqvist H, Langsrom BB, Mosskin M (1985) Positron emission tomography with ([11C]methyl)-l-methionine, [11C]d-glucose, and [68 Ga]EDTA in supratentorial tumors. J Comput Assist Tomogr 9:683–689PubMedCrossRef
18.
go back to reference Herholz K, Holzer T, Bauer B, Schroder R, Voges J, Ernestus RI, Mendoza G, Weber-Luxenburger G, Lottgen J, Thiel A, Wienhard K, Heiss WD (1998) 11C-Methionine PET for differential diagnosis of low-grade gliomas. Neurology 50:1316–1322PubMedCrossRef Herholz K, Holzer T, Bauer B, Schroder R, Voges J, Ernestus RI, Mendoza G, Weber-Luxenburger G, Lottgen J, Thiel A, Wienhard K, Heiss WD (1998) 11C-Methionine PET for differential diagnosis of low-grade gliomas. Neurology 50:1316–1322PubMedCrossRef
19.
go back to reference Kracht LW, Miletic H, Busch S, Jacobs AH, Voges J, Hoevels M, Klein JC, Herholz K, Heiss WD (2004) Delineation of brain tumor extent with [11C]l-methionine positron emission tomography: local comparison with stereotactic histopathology. Clin Cancer Res 10:7163–7170. doi:10.1158/1078-0432.CCR-04-0262 PubMedCrossRef Kracht LW, Miletic H, Busch S, Jacobs AH, Voges J, Hoevels M, Klein JC, Herholz K, Heiss WD (2004) Delineation of brain tumor extent with [11C]l-methionine positron emission tomography: local comparison with stereotactic histopathology. Clin Cancer Res 10:7163–7170. doi:10.​1158/​1078-0432.​CCR-04-0262 PubMedCrossRef
20.
go back to reference Ribom D, Eriksson A, Hartman M, Engler H, Nilsson A, Langstrom B, Bolander H, Bergstrom M, Smits A (2001) Positron emission tomography (11)C-methionine and survival in patients with low-grade gliomas. Cancer 92:1541–1549. doi:10.1002/1097-0142(20010915)92 PubMedCrossRef Ribom D, Eriksson A, Hartman M, Engler H, Nilsson A, Langstrom B, Bolander H, Bergstrom M, Smits A (2001) Positron emission tomography (11)C-methionine and survival in patients with low-grade gliomas. Cancer 92:1541–1549. doi:10.​1002/​1097-0142(20010915)92 PubMedCrossRef
21.
go back to reference Knopp EA, Cha S, Johnson G, Mazumdar A, Golfinos JG, Zagzag D, Miller DC, Kelly PJ, Kricheff II (1999) Glial neoplasms: dynamic contrast-enhanced T2*-weighted MR imaging. Radiology 211:791–798PubMed Knopp EA, Cha S, Johnson G, Mazumdar A, Golfinos JG, Zagzag D, Miller DC, Kelly PJ, Kricheff II (1999) Glial neoplasms: dynamic contrast-enhanced T2*-weighted MR imaging. Radiology 211:791–798PubMed
22.
go back to reference Boxerman JL, Schmainda KM, Weisskoff RM (2006) Relative cerebral blood volume maps corrected for contrast agent extravasation significantly correlate with glioma tumor grade, whereas uncorrected maps do not. AJNR Am J Neuroradiol 27:859–867PubMed Boxerman JL, Schmainda KM, Weisskoff RM (2006) Relative cerebral blood volume maps corrected for contrast agent extravasation significantly correlate with glioma tumor grade, whereas uncorrected maps do not. AJNR Am J Neuroradiol 27:859–867PubMed
24.
go back to reference Vrabec M, Van Cauter S, Himmelreich U, Van Gool SW, Sunaert S, De Vleeschouwer S, Suput D, Demaerel P (2011) MR perfusion and diffusion imaging in the follow-up of recurrent glioblastoma treated with dendritic cell immunotherapy: a pilot study. Neuroradiology 53:721–731. doi:10.1007/s00234-010-0802-6 PubMedCrossRef Vrabec M, Van Cauter S, Himmelreich U, Van Gool SW, Sunaert S, De Vleeschouwer S, Suput D, Demaerel P (2011) MR perfusion and diffusion imaging in the follow-up of recurrent glioblastoma treated with dendritic cell immunotherapy: a pilot study. Neuroradiology 53:721–731. doi:10.​1007/​s00234-010-0802-6 PubMedCrossRef
25.
go back to reference Alyafei S, Inoue T, Zhang H, Ahmed K, Oriuchi N, Sato N, Suzuki H, Endo K (1999) Image fusion system using PACS for MRI, CT, and PET images. Clin Positron Imaging 2:137–143PubMedCrossRef Alyafei S, Inoue T, Zhang H, Ahmed K, Oriuchi N, Sato N, Suzuki H, Endo K (1999) Image fusion system using PACS for MRI, CT, and PET images. Clin Positron Imaging 2:137–143PubMedCrossRef
27.
go back to reference Lilja A, Bergstrom K, Hartvig P, Spannare B, Halldin C, Lundqvist H, Langstrom B (1985) Dynamic study of supratentorial gliomas with L-methyl-11C-methionine and positron emission tomography. AJNR Am J Neuroradiol 6:505–514PubMed Lilja A, Bergstrom K, Hartvig P, Spannare B, Halldin C, Lundqvist H, Langstrom B (1985) Dynamic study of supratentorial gliomas with L-methyl-11C-methionine and positron emission tomography. AJNR Am J Neuroradiol 6:505–514PubMed
28.
go back to reference Van Laere K, Ceyssens S, Van Calenbergh F, de Groot T, Menten J, Flamen P, Bormans G, Mortelmans L (2005) Direct comparison of 18F-FDG and 11C-methionine PET in suspected recurrence of glioma: sensitivity, inter-observer variability and prognostic value. Eur J Nucl Med Mol Imaging 32:39–51. doi:10.1007/s00259-004-1564-3 PubMedCrossRef Van Laere K, Ceyssens S, Van Calenbergh F, de Groot T, Menten J, Flamen P, Bormans G, Mortelmans L (2005) Direct comparison of 18F-FDG and 11C-methionine PET in suspected recurrence of glioma: sensitivity, inter-observer variability and prognostic value. Eur J Nucl Med Mol Imaging 32:39–51. doi:10.​1007/​s00259-004-1564-3 PubMedCrossRef
29.
30.
go back to reference Murakami R, Hirai T, Sugahara T, Fukuoka H, Toya R, Nishimura S, Kitajima M, Okuda T, Nakamura H, Oya N, Kuratsu J, Yamashita Y (2009) Grading astrocytic tumors by using apparent diffusion coefficient parameters: superiority of a one-versus two-parameter pilot method. Radiology 251:838–845. doi:10.1148/radiol.2513080899 PubMedCrossRef Murakami R, Hirai T, Sugahara T, Fukuoka H, Toya R, Nishimura S, Kitajima M, Okuda T, Nakamura H, Oya N, Kuratsu J, Yamashita Y (2009) Grading astrocytic tumors by using apparent diffusion coefficient parameters: superiority of a one-versus two-parameter pilot method. Radiology 251:838–845. doi:10.​1148/​radiol.​2513080899 PubMedCrossRef
31.
go back to reference Sadeghi N, Salmon I, Tang BN, Denolin V, Levivier M, Wikler D, Rorive S, Baleriaux D, Metens T, Goldman S (2006) Correlation between dynamic susceptibility contrast perfusion MRI and methionine metabolism in brain gliomas: preliminary results. J Magn Reson Imaging 24:989–994. doi:10.1002/jmri.20757 PubMedCrossRef Sadeghi N, Salmon I, Tang BN, Denolin V, Levivier M, Wikler D, Rorive S, Baleriaux D, Metens T, Goldman S (2006) Correlation between dynamic susceptibility contrast perfusion MRI and methionine metabolism in brain gliomas: preliminary results. J Magn Reson Imaging 24:989–994. doi:10.​1002/​jmri.​20757 PubMedCrossRef
32.
go back to reference Caseiras GB, Thornton JS, Yousry T, Benton C, Rees J, Waldman AD, Jager HR (2008) Inclusion or exclusion of intratumoral vessels in relative cerebral blood volume characterization in low-grade gliomas: does it make a difference? AJNR Am J Neuroradiol 29:1140–1141. doi:10.3174/ajnr.A0993 PubMedCrossRef Caseiras GB, Thornton JS, Yousry T, Benton C, Rees J, Waldman AD, Jager HR (2008) Inclusion or exclusion of intratumoral vessels in relative cerebral blood volume characterization in low-grade gliomas: does it make a difference? AJNR Am J Neuroradiol 29:1140–1141. doi:10.​3174/​ajnr.​A0993 PubMedCrossRef
34.
go back to reference Scott JN, Brasher PM, Sevick RJ, Rewcastle NB, Forsyth PA (2002) How often are nonenhancing supratentorial gliomas malignant? A population study. Neurology 59:947–949PubMedCrossRef Scott JN, Brasher PM, Sevick RJ, Rewcastle NB, Forsyth PA (2002) How often are nonenhancing supratentorial gliomas malignant? A population study. Neurology 59:947–949PubMedCrossRef
35.
go back to reference Law M, Young RJ, Babb JS, Peccerelli N, Chheang S, Gruber ML, Miller DC, Golfinos JG, Zagzag D, Johnson G (2008) Gliomas: predicting time to progression or survival with cerebral blood volume measurements at dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging. Radiology 247:490–498. doi:10.1148/radiol.2472070898 PubMedCrossRef Law M, Young RJ, Babb JS, Peccerelli N, Chheang S, Gruber ML, Miller DC, Golfinos JG, Zagzag D, Johnson G (2008) Gliomas: predicting time to progression or survival with cerebral blood volume measurements at dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging. Radiology 247:490–498. doi:10.​1148/​radiol.​2472070898 PubMedCrossRef
36.
go back to reference Jenkinson MD, Smith TS, Joyce KA, Fildes D, Broome J, du Plessis DG, Haylock B, Husband DJ, Warnke PC, Walker C (2006) Cerebral blood volume, genotype and chemosensitivity in oligodendroglial tumours. Neuroradiology 48:703–713. doi:10.1007/s00234-006-0122-z PubMedCrossRef Jenkinson MD, Smith TS, Joyce KA, Fildes D, Broome J, du Plessis DG, Haylock B, Husband DJ, Warnke PC, Walker C (2006) Cerebral blood volume, genotype and chemosensitivity in oligodendroglial tumours. Neuroradiology 48:703–713. doi:10.​1007/​s00234-006-0122-z PubMedCrossRef
37.
go back to reference Thomsen H, Steffensen E, Larsson EM (2012) Perfusion MRI (dynamic susceptibility contrast imaging) with different measurement approaches for the evaluation of blood flow and blood volume in human gliomas. Acta Radiol 53:95–101. doi:10.1258/ar.2011.110242 PubMedCrossRef Thomsen H, Steffensen E, Larsson EM (2012) Perfusion MRI (dynamic susceptibility contrast imaging) with different measurement approaches for the evaluation of blood flow and blood volume in human gliomas. Acta Radiol 53:95–101. doi:10.​1258/​ar.​2011.​110242 PubMedCrossRef
38.
go back to reference Lee EJ, Lee SK, Agid R, Bae JM, Keller A, Terbrugge K (2008) Preoperative grading of presumptive low-grade astrocytomas on MR imaging: diagnostic value of minimum apparent diffusion coefficient. AJNR Am J Neuroradiol 29:1872–1877. doi:10.3174/ajnr.A1254 PubMedCrossRef Lee EJ, Lee SK, Agid R, Bae JM, Keller A, Terbrugge K (2008) Preoperative grading of presumptive low-grade astrocytomas on MR imaging: diagnostic value of minimum apparent diffusion coefficient. AJNR Am J Neuroradiol 29:1872–1877. doi:10.​3174/​ajnr.​A1254 PubMedCrossRef
39.
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 13:447–455. doi:10.1093/neuonc/noq197 PubMedCrossRef 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 13:447–455. doi:10.​1093/​neuonc/​noq197 PubMedCrossRef
Metadata
Title
Perfusion and diffusion MRI combined with 11C-methionine PET in the preoperative evaluation of suspected adult low-grade gliomas
Authors
Shala Ghaderi Berntsson
Anna Falk
Irina Savitcheva
Andrea Godau
Maria Zetterling
Göran Hesselager
Irina Alafuzoff
Elna-Marie Larsson
Anja Smits
Publication date
01-09-2013
Publisher
Springer US
Published in
Journal of Neuro-Oncology / Issue 2/2013
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI
https://doi.org/10.1007/s11060-013-1178-3

Other articles of this Issue 2/2013

Journal of Neuro-Oncology 2/2013 Go to the issue