Abstract
Target population
These recommendations apply to adults with glioblastoma who have been previously treated with first-line radiation or chemoradiotherapy and who are suspected of experiencing tumor progression.
Question: In patients with previously treated glioblastoma, is standard contrast-enhanced magnetic resonance imaging including diffusion weighted imaging useful for diagnosing tumor progression and differentiating progression from treatment-related changes?
Level II: Magnetic resonance imaging with and without gadolinium enhancement including diffusion weighted imaging is recommended as the imaging surveillance method to detect the progression of previously diagnosed glioblastoma.
Question: In patients with previously treated glioblastoma, does magnetic resonance spectroscopy add useful information for diagnosing tumor progression and differentiating progression from treatment-related changes beyond that derived from standard magnetic resonance imaging with and without gadolinium enhancement?
Level II: Magnetic resonance spectroscopy is recommended as a diagnostic method to differentiate true tumor progression from treatment-related imaging changes or pseudo-progression in patients with suspected progressive glioblastoma.
Question: In patients with previously treated glioblastoma, does magnetic resonance perfusion add useful information for diagnosing tumor progression and differentiating progression from treatment-related changes beyond that derived from standard magnetic resonance imaging with and without gadolinium enhancement?
Level III: Magnetic resonance perfusion is suggested as a diagnostic method to differentiate true tumor progression from treatment-related imaging changes or pseudo-progression in patients with suspected progressive glioblastoma.
Question: In patients with previously treated glioblastoma, does the addition of single-photon emission computed tomography (SPECT) provide additional useful information for diagnosing tumor progression and differentiating progression from treatment-related changes beyond that derived from standard magnetic resonance imaging with and without gadolinium enhancement?
Level III: Single-photon emission computed tomography imaging is suggested as a diagnostic method to differentiate true tumor progression from treatment-related imaging changes or pseudo-progression in patients with suspected progressive glioblastoma.
Question: In patients with previously treated glioblastoma, does 18F-fluorodeoxyglucose positron emission tomography add useful information for diagnosing tumor progression and differentiating progression from treatment-related changes beyond that derived from standard magnetic resonance imaging with and without gadolinium enhancement?
Level III: The routine use of 18F-fluorodeoxyglucose positron emission tomography to identify progression of glioblastoma is not recommended.
Question: In patients with previously treated glioblastoma, does positron emission tomography with amino acid agents add useful information for diagnosing tumor progression and differentiating progression from treatment-related changes beyond that derived from standard magnetic resonance imaging with and without gadolinium enhancement?
Level III: It is suggested that amino acid positron emission tomography be considered to assist in the differentiation of progressive glioblastoma from treatment related changes.
Similar content being viewed by others
Data availability
The data generated during and/or analyzed during the current study are available via www.cns.org/guidelines.
Abbreviations
- AA:
-
Amino acid
- AANS:
-
American Association of Neurological Surgeons
- AMT:
-
α-[11C]-methyl-l-tryptophan
- ADC:
-
Apparent diffusion coefficient
- AUC:
-
Area under the curve
- ceMR:
-
Contrast-enhanced magnetic resonance imaging
- CBV:
-
Cerebral blood volume
- CI:
-
Confidence interval
- CNS:
-
Congress of neurological surgeons
- DCE:
-
Dynamic contrast enhanced
- DSC:
-
Dynamic susceptibility contrast
- DWI:
-
Diffusion weighted imaging
- FDOPA:
-
3,4-Dihydroxy-6-[18F]-fluoro-l-phenylalanine
- FET:
-
O-(2-[18F]-fluoroethyl)- l -tyrosine
- FLT:
-
18F-fluorothymidine
- FDG:
-
18F-fluorodeoxyglucose
- HGG:
-
High-grade glioma
- IDH:
-
Isocitrate dehydrogenase
- MET:
-
11C-methyl-methionine
- MR:
-
Magnetic resonance
- MRS:
-
Magnetic resonance spectroscopy
- NAA:
-
N-acetylaspartate
- OS:
-
Overall survival
- PET:
-
Positron emission tomography
- PFS:
-
Progression free survival
- RANO:
-
Response assessment in neuro-oncology
- rCBV:
-
Relative cerebral blood volume
- SPECT:
-
Single photon emission computed tomography
- VEGF:
-
Vascular endothelial growth factor
References
Ryken TC, Aygun N, Morris J et al (2014) The role of imaging in the management of progressive glioblastoma: a systematic review and evidence-based clinical practice guideline. J Neurooncol 118:435–460
Congress of Neurologic Surgeons (2020) Guideline development methodology. https://www.cns.org/guidelines/guideline-development-methodology. Accessed 1 Feb 2020
van Dijken BRJ, van Laar PJ, Holtman GA, van der Hoorn A (2017) Diagnostic accuracy of magnetic resonance imaging techniques for treatment response evaluation in patients with high-grade glioma, a systematic review and meta-analysis. Eur Radiol 27:4129–4144
Ellingson BM, Aftab DT, Schwab GM et al (2018) Volumetric response quantified using T1 subtraction predicts long-term survival benefit from cabozantinib monotherapy in recurrent glioblastoma. Neuro Oncol 20:1411–1418
Ellingson BM, Kim HJ, Woodworth DC et al (2014) Recurrent glioblastoma treated with bevacizumab: contrast-enhanced T1-weighted subtraction maps improve tumor delineation and aid prediction of survival in a multicenter clinical trial. Radiology 271:200–210
Lescher S, Jurcoane A, Veit A, Bähr O, Deichmann R, Hattingen E (2015) Quantitative T1 and T2 mapping in recurrent glioblastomas under bevacizumab: earlier detection of tumor progression compared to conventional MRI. Neuroradiology 57:11–20
Ellingson BM, Lai A, Nguyen HN, Nghiemphu PL, Pope WB, Cloughesy TF (2015) Quantification of nonenhancing tumor burden in gliomas using effective T2 maps derived from dual-echo turbo spin-echo MRI. Clin Cancer Res 21:4373–4383
Hattingen E, Jurcoane A, Daneshvar K et al (2013) Quantitative T2 mapping of recurrent glioblastoma under bevacizumab improves monitoring for non-enhancing tumor progression and predicts overall survival. Neuro Oncol 15:1395–1404
Schaub C, Greschus S, Seifert M et al (2013) FLAIR-only progression in bevacizumab-treated relapsing glioblastoma does not predict short survival. Oncology 85:191–195
Nguyen HS, Milbach N, Hurrell SL et al (2016) Progressing bevacizumab-induced diffusion restriction is associated with coagulative necrosis surrounded by viable tumor and decreased overall survival in patients with recurrent glioblastoma. AJNR Am J Neuroradiol 37:2201–2208
Auer TA, Breit HC, Marini F et al (2019) Evaluation of the apparent diffusion coefficient in patients with recurrent glioblastoma under treatment with bevacizumab with radiographic pseudoresponse. J Neuroradiol 46:36–43
Ellingson BM, Kim E, Woodworth DC et al (2015) Diffusion MRI quality control and functional diffusion map results in ACRIN 6677/RTOG 0625: a multicenter, randomized, phase II trial of bevacizumab and chemotherapy in recurrent glioblastoma. Int J Oncol 46:1883–1892
Ellingson BM, Gerstner ER, Smits M et al (2017) Diffusion MRI phenotypes predict overall survival benefit from anti-VEGF monotherapy in recurrent glioblastoma: converging evidence from phase II trials. Clin Cancer Res 23:5745–5756
Zhang H, Ma L, Wang Q, Zheng X, Wu C, Xu BN (2014) Role of magnetic resonance spectroscopy for the differentiation of recurrent glioma from radiation necrosis: a systematic review and meta-analysis. Eur J Radiol 83:2181–2189
Kazda T, Bulik M, Pospisil P et al (2016) Advanced MRI increases the diagnostic accuracy of recurrent glioblastoma: single institution thresholds and validation of MR spectroscopy and diffusion weighted MR imaging. Neuroimage Clin 11:316–321
Steidl E, Pilatus U, Hattingen E et al (2016) Myoinositol as a biomarker in recurrent glioblastoma treated with bevacizumab: a 1H-magnetic resonance spectroscopy study. PLoS One 11:e0168113
Beppu T, Sato Y, Sasaki T et al (2019) Comparisons between PET With 11C-methyl-l-methionine and arterial spin labeling perfusion imaging in recurrent glioblastomas treated with bevacizumab. Clin Nucl Med 44:186–193
Hojjati M, Badve C, Garg V et al (2018) Role of FDG-PET/MRI, FDG-PET/CT, and dynamic susceptibility contrast perfusion mri in differentiating radiation necrosis from tumor recurrence in glioblastomas. J Neuroimaging 28:118–125
Thomas AA, Arevalo-Perez J, Kaley T et al (2015) Dynamic contrast enhanced T1 MRI perfusion differentiates pseudoprogression from recurrent glioblastoma. J Neurooncol 125:183–190
Hu LS, Eschbacher JM, Heiserman JE et al (2012) Reevaluating the imaging definition of tumor progression: perfusion MRI quantifies recurrent glioblastoma tumor fraction, pseudoprogression, and radiation necrosis to predict survival. Neuro Oncol 14:919–930
Di Costanzo A, Scarabino T, Trojsi F et al (2014) Recurrent glioblastoma multiforme versus radiation injury: a multiparametric 3-T MR approach. Radiol Med 119:616–624
Kim HS, Goh MJ, Kim N, Choi CG, Kim SJ, Kim JH (2014) Which combination of MR imaging modalities is best for predicting recurrent glioblastoma? Study of diagnostic accuracy and reproducibility. Radiology 273:831–843
Kickingereder P, Wiestler B, Burth S et al (2015) Relative cerebral blood volume is a potential predictive imaging biomarker of bevacizumab efficacy in recurrent glioblastoma. Neuro Oncol 17:1139–1147
Bennett IE, Field KM, Hovens CM et al (2017) Early perfusion MRI predicts survival outcome in patients with recurrent glioblastoma treated with bevacizumab and carboplatin. J Neurooncol 131:321–329
Kickingereder P, Radbruch A, Burth S et al (2016) MR perfusion-derived hemodynamic parametric response mapping of bevacizumab efficacy in recurrent glioblastoma. Radiology 279:542–552
Kickingereder P, Wiestler B, Graf M et al (2015) Evaluation of dynamic contrast-enhanced MRI derived microvascular permeability in recurrent glioblastoma treated with bevacizumab. J Neurooncol 121:373–380
Schmainda KM, Zhang Z, Prah M et al (2015) Dynamic susceptibility contrast MRI measures of relative cerebral blood volume as a prognostic marker for overall survival in recurrent glioblastoma: results from the ACRIN 6677/RTOG 0625 multicenter trial. Neuro Oncol 17:1148–1156
Hilario A, Sepulveda JM, Hernandez-Lain A et al (2017) Leakage decrease detected by dynamic susceptibility-weighted contrast-enhanced perfusion MRI predicts survival in recurrent glioblastoma treated with bevacizumab. Clin Transl Oncol 19:51–57
Stecco A, Amatuzzo P, Sponghini AP et al (2019) Prognostic value of relative cerebral blood volume in patients with recurrent glioblastoma multiforme treated with bevacizumab. J Neurosurg Sci 63:394–401
Leu K, Enzmann DR, Woodworth DC et al (2014) Hypervascular tumor volume estimated by comparison to a large-scale cerebral blood volume radiographic atlas predicts survival in recurrent glioblastoma treated with bevacizumab. Cancer Imaging 14:31
Stadlbauer A, Pichler P, Karl M et al (2015) Quantification of serial changes in cerebral blood volume and metabolism in patients with recurrent glioblastoma undergoing antiangiogenic therapy. Eur J Radiol 84:1128–1136
Leu K, Boxerman JL, Lai A et al (2016) Bidirectional Contrast agent leakage correction of dynamic susceptibility contrast (DSC)-MRI improves cerebral blood volume estimation and survival prediction in recurrent glioblastoma treated with bevacizumab. J Magn Reson Imaging 44:1229–1237
Patel P, Baradaran H, Delgado D et al (2017) MR perfusion-weighted imaging in the evaluation of high-grade gliomas after treatment: a systematic review and meta-analysis. Neuro Oncol 19:118–127
Patronas NJ, Di Chiro G, Brooks RA et al (1982) Work in progress: [18F] fluorodeoxyglucose and positron emission tomography in the evaluation of radiation necrosis of the brain. Radiology 144:885–889
Leiva-Salinas C, Schiff D, Flors L, Patrie JT, Rehm PK (2017) FDG PET/MR imaging coregistration helps predict survival in patients with glioblastoma and radiologic progression after standard of care treatment. Radiology 283:508–514
Karunanithi S, Sharma P, Kumar A et al (2013) 18F-FDOPA PET/CT for detection of recurrence in patients with glioma: prospective comparison with 18F-FDG PET/CT. Eur J Nucl Med Mol Imaging 40:1025–1035
Hassanzadeh C, Rao YJ, Chundury A et al (2017) Multiparametric MRI and [(18)F]fluorodeoxyglucose positron emission tomography imaging is a potential prognostic imaging biomarker in recurrent glioblastoma. Front Oncol 7:178
Beppu T, Terasaki K, Sasaki T et al (2016) MRI and 11C-methyl-l-methionine PET differentiate bevacizumab true responders after initiating therapy for recurrent glioblastoma. Clin Nucl Med 41:852–857
Deuschl C, Kirchner J, Poeppel TD et al (2018) (11)C-MET PET/MRI for detection of recurrent glioma. Eur J Nucl Med Mol Imaging 45:593–601
Sharma R, D’Souza M, Jaimini A et al (2016) A comparison study of (11)C-methionine and (18)F-fluorodeoxyglucose positron emission tomography-computed tomography scans in evaluation of patients with recurrent brain tumors. Indian J Nucl Med 31:93–102
Takenaka S, Asano Y, Shinoda J et al (2014) Comparison of (11)C-methionine, (11)C-choline, and (18)F-fluorodeoxyglucose-PET for distinguishing glioma recurrence from radiation necrosis. Neurol Med Chir (Tokyo) 54:280–289
Evangelista L, Cuppari L, Bellu L et al (2019) Comparison between 18F-dopa and 18F-Fet PET/CT in patients with suspicious recurrent high grade glioma: a literature review and our experience. Curr Radiopharm 12:220–228
Kebir S, Fimmers R, Galldiks N et al (2016) Late pseudoprogression in glioblastoma: diagnostic value of dynamic O-(2-[18F]fluoroethyl)-l-tyrosine PET. Clin Cancer Res 22:2190–2196
Galldiks N, Dunkl V, Stoffels G et al (2015) Diagnosis of pseudoprogression in patients with glioblastoma using O-(2-[18F]fluoroethyl)-l-tyrosine PET. Eur J Nucl Med Mol Imaging 42:685–695
Galldiks N, Rapp M, Stoffels G et al (2013) Response assessment of bevacizumab in patients with recurrent malignant glioma using [18F]Fluoroethyl-l-tyrosine PET in comparison to MRI. Eur J Nucl Med Mol Imaging 40:22–33
George E, Kijewski MF, Dubey S et al (2018) Voxel-wise analysis of fluoroethyltyrosine PET and MRI in the assessment of recurrent glioblastoma during antiangiogenic therapy. AJR Am J Roentgenol 211:1342–1347
Sogani SK, Jena A, Taneja S et al (2017) Potential for differentiation of glioma recurrence from radionecrosis using integrated (18)F-fluoroethyl-l-tyrosine (FET) positron emission tomography/magnetic resonance imaging: a prospective evaluation. Neurol India 65:293–301
Jena A, Taneja S, Gambhir A et al (2016) Glioma recurrence versus radiation necrosis: single-session multiparametric approach using simultaneous O-(2–18F-Fluoroethyl)-l-tyrosine PET/MRI. Clin Nucl Med 41:e228-236
Pyka T, Hiob D, Preibisch C et al (2018) Diagnosis of glioma recurrence using multiparametric dynamic 18F-fluoroethyl-tyrosine PET-MRI. Eur J Radiol 103:32–37
Verger A, Filss CP, Lohmann P et al (2018) Comparison of O-(2-(18)F-fluoroethyl)-l-tyrosine positron emission tomography and perfusion-weighted magnetic resonance imaging in the diagnosis of patients with progressive and recurrent glioma: a hybrid positron emission tomography/magnetic resonance study. World Neurosurg 113:e727–e737
Humbert O, Bourg V, Mondot L et al (2019) (18)F-DOPA PET/CT in brain tumors: impact on multidisciplinary brain tumor board decisions. Eur J Nucl Med Mol Imaging 46:558–568
Karunanithi S, Bandopadhyaya GP, Sharma P et al (2014) Prospective comparison of (99m)Tc-GH SPECT/CT and (18)F-FDOPA PET/CT for detection of recurrent glioma: a pilot study. Clin Nucl Med 39:e121-128
Karunanithi S, Sharma P, Kumar A et al (2013) Comparative diagnostic accuracy of contrast-enhanced MRI and (18)F-FDOPA PET-CT in recurrent glioma. Eur Radiol 23:2628–2635
Youland RS, Pafundi DH, Brinkmann DH et al (2018) Prospective trial evaluating the sensitivity and specificity of 3,4-dihydroxy-6-[18F]-fluoro-l-phenylalanine (18F-DOPA) PET and MRI in patients with recurrent gliomas. J Neurooncol 137:583–591
Brahm CG, den Hollander MW, Enting RH et al (2018) Serial FLT PET imaging to discriminate between true progression and pseudoprogression in patients with newly diagnosed glioblastoma: a long-term follow-up study. Eur J Nucl Med Mol Imaging 45:2404–2412
Bosnyák E, Kamson DO, Robinette NL, Barger GR, Mittal S, Juhász C (2016) Tryptophan PET predicts spatial and temporal patterns of post-treatment glioblastoma progression detected by contrast-enhanced MRI. J Neurooncol 126:317–325
Langen KJ, Tonn JC, Weller M, Galldiks N (2014) Letter to the Editor: “The role of imaging in the management of progressive glioblastoma. A systematic review and evidence-based clinical practice guideline” [J Neurooncol 2014; 118:435–460]. J Neurooncol 120:665–666
Holdhoff M, Ye X, Piotrowski AF et al (2019) The consistency of neuropathological diagnoses in patients undergoing surgery for suspected recurrence of glioblastoma. J Neurooncol 141:347–354
Chung WJ, Kim HS, Kim N, Choi CG, Kim SJ (2013) Recurrent glioblastoma: optimum area under the curve method derived from dynamic contrast-enhanced T1-weighted perfusion MR imaging. Radiology 269:561–568
Acknowledgements
The guidelines task force would like to acknowledge the Congress of Neurological Surgeons Guidelines Committee for their contributions throughout the development of the guideline, and the American Association of Neurological Surgeons/Congress of Neurological Surgeons Joint Guidelines Review Committee for their review, comments, and suggestions throughout peer review, as well as the contributions of Trish Rehring, MPH, CHES, Senior Manager of Clinical Practice Guidelines for the CNS, and Mary Bodach, MLIS, from the Congress of Neurological Surgeons Guidelines Office for organizational assistance and reference librarian services, respectively as well as Jeremy Kupsco, PhD, Informationist, Emory University, for their valuable input as Medical Research Librarians. Throughout the review process, the reviewers and authors were blinded from one another. At this time the guidelines task force would like to acknowledge the following individual peer reviewers for their contributions: John O’Toole, MD, Brian Howard, MD, Jamie Van Gompel, MD, Howard Silberstein, MD, Navid Redjal, MD and Shawn Hervey-Jumper, MD.
Funding
These guidelines were funded exclusively by the Congress of Neurological Surgery and the Joint Section on Tumors of the Congress of Neurological Surgeons and the American Association of Neurological Surgeons, which received no funding from any outside commercial sources to support the development of this document.
Author information
Authors and Affiliations
Contributions
The author listed on this publication agrees with the content included and gives explicit consent to the submission of this publication. The author obtained consent from the responsible authorities at the institute/organization where the work has been carried out, before the work was submitted. The author whose name appear on this submission: (1) made substantial contributions to the conception or design of the work; or the acquisition, analysis, or interpretation of data; or the creation of new software used in the work; (2) drafted the work or revised it critically for important intellectual content; (3) approved the version to be published; and (4) agreed to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.
Corresponding author
Ethics declarations
Conflict of interest
All Guideline Task Force members were required to disclose all potential COIs prior to beginning work on the guideline, using the COI disclosure form of the AANS/CNS Joint Guidelines Review Committee. The CNS Guidelines Committee and Guideline Task Force Chair reviewed the disclosures and either approved or disapproved the nomination and participation on the task force. The CNS Guidelines Committee and Guideline Task Force Chair may approve nominations of task force members with possible conflicts and restrict the writing, reviewing, and/or voting privileges of that person to topics that are unrelated to the possible COIs. The authors have no personal, financial, or institutional interest in any of the drugs, materials, or devices described in this series of articles.
Data transparency
The author has ensured all data and materials as well as software applications or custom code supports their published claims and comply with field standards.
Ethical approval
This article does not contain any studies with human participants performed by any of the authors.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Sponsors: Congress of Neurological Surgeons (CNS) and the Section on Tumors.
Endorsement: Reviewed for evidence-based integrity and endorsed by the American Association of Neurological Surgeons and Congress of Neurological Surgeons.
Rights and permissions
About this article
Cite this article
Johnson, D.R., Glenn, C.A., Javan, R. et al. Congress of Neurological Surgeons systematic review and evidence-based guidelines update on the role of imaging in the management of progressive glioblastoma in adults. J Neurooncol 158, 139–165 (2022). https://doi.org/10.1007/s11060-021-03853-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11060-021-03853-0