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      Incidence of Tumour Progression and Pseudoprogression in High-Grade Gliomas: a Systematic Review and Meta-Analysis

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          Abstract

          Background

          High-grade gliomas are the most common primary brain tumours. Pseudoprogression describes the false appearance of radiation-induced progression on MRI. A distinction should be made from true tumour progression to correctly plan treatment. However, there is wide variation of reported pseudoprogression. We thus aimed to establish the incidence of pseudoprogression and tumour progression in high-grade glioma patients with a systematic review and meta-analysis.

          Methods

          We searched PubMed, Embase and Web of Science on the incidence of pseudoprogression and tumour progression in adult high-grade glioma patients from 2005, the latest on 8 October 2014. Histology or imaging follow-up was used as reference standard. Extracted data included number of patients with worsening of imaging findings on T1 postcontrast or T2/FLAIR, pseudoprogression and tumour progression. Study quality was assessed. Heterogeneity was tested with I 2 . Pooling of the results was done with random models using Metaprop in STATA (StataCorp. Stata Statistical Software. College Station, TX: StataCorp LP).

          Results

          We identified 73 studies. MRI progression occurred in 2603 patients. Of these, 36% (95% confidence interval [CI] 33–40%) demonstrated pseudoprogression, 60% (95%CI 56–64%) tumour progression and unknown outcome was present in the remaining 4% of the patients (range 1–37%).

          Conclusion

          This meta-analysis demonstrated for the first time a notably high pooled incidence of pseudoprogression in patients with a form of progression across the available literature. This highlighted the full extent of the problem of the currently conventional MRI-based Response Assessment in Neuro-Oncology (RANO) criteria for treatment evaluation in high-grade gliomas. This underscores the need for more accurate treatment evaluation using advanced imaging to improve diagnostic accuracy and therapeutic approach.

          Electronic supplementary material

          The online version of this article (doi: 10.1007/s00062-017-0584-x) contains supplementary material, which is available to authorized users. It contains the characteristics of the included studies (supplementary table 1) and a full search strategy (see supplementary search strategy).

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          Most cited references79

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          MGMT promoter methylation status can predict the incidence and outcome of pseudoprogression after concomitant radiochemotherapy in newly diagnosed glioblastoma patients.

          Standard therapy for glioblastoma (GBM) is temozolomide (TMZ) administration, initially concurrent with radiotherapy (RT), and subsequently as maintenance therapy. The radiologic images obtained in this setting can be difficult to interpret since they may show radiation-induced pseudoprogression (psPD) rather than disease progression. Patients with histologically confirmed GBM underwent radiotherapy plus continuous daily temozolomide (75 mg/m(2)/d), followed by 12 maintenance temozolomide cycles (150 to 200 mg/m(2) for 5 days every 28 days) if magnetic resonance imaging (MRI) showed no enhancement suggesting a tumor; otherwise, chemotherapy was delivered until complete response or unequivocal progression. The first MRI scan was performed 1 month after completing combined chemoradiotherapy. In 103 patients (mean age, 52 years [range 20 to 73 years]), total resection, subtotal resection, and biopsy were obtained in 51, 51, and 1 cases, respectively. MGMT promoter was methylated in 36 patients (35%) and unmethylated in 67 patients (65%). Lesion enlargement, evidenced at the first MRI scan in 50 of 103 patients, was subsequently classified as psPD in 32 patients and early disease progression in 18 patients. PsPD was recorded in 21 (91%) of 23 methylated MGMT promoter and 11 (41%) of 27 unmethylated MGMT promoter (P = .0002) patients. MGMT status (P = .001) and psPD detection (P = .045) significantly influenced survival. PsPD has a clinical impact on chemotherapy-treated GBM, as it may express the glioma killing effects of treatment and is significantly correlated with MGMT status. Improvement in the early recognition of psPD patterns and knowledge of mechanisms underlying this phenomenon are crucial to eliminating biases in evaluating the results of clinical trials and guaranteeing effective treatment.
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            Radiation-induced dementia in patients cured of brain metastases.

            When a patient with cancer develops a brain metastasis, death is usually imminent, but aggressive treatment in some patients with limited or no systemic disease yields long-term survival. In such patients, delayed deleterious effects of therapy are particularly tragic. We report 12 patients who developed delayed complications of whole brain radiotherapy (WBRT) given as sole treatment (4 patients) or in combination with surgical resection (8 patients). Within 5 to 36 months (median, 14) all patients developed progressive dementia, ataxia, and urinary incontinence causing severe disability in all and leading to death in 7. No patient had tumor recurrence when neurologic symptoms began. Cortical atrophy and hypodense white matter were identified by CT in all. Contrast-enhancing lesions were seen in 3 patients; 2 of the lesions yielded radionecrosis on biopsy. Autopsies on 2 patients revealed diffuse chronic edema of the hemispheric white matter in the absence of tumor recurrence. Corticosteroids and ventriculoperitoneal shunt offered significant but incomplete improvement in some patients. The total dose of WBRT was only 2,500 to 3,900 cGy, but daily fractions of 300 to 600 cGy were employed. We believe that these fractionation schedules, several of which are used commonly, predispose to delayed neurologic toxicity, and that more protracted schedules should be employed for the safe and efficacious treatment of good-risk patients with brain metastases. The incidence of WBRT-induced dementia was only 1.9 to 5.1% in the 2 populations reviewed here; however, this underestimates the incidence because only severely affected patients could be identified from chart review.
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              Differentiation of recurrent glioblastoma multiforme from radiation necrosis after external beam radiation therapy with dynamic susceptibility-weighted contrast-enhanced perfusion MR imaging.

              To investigate whether cerebral blood volume (CBV), peak height (PH), and percentage of signal intensity recovery (PSR) measurements derived from the results of T2-weighted dynamic susceptibility-weighted contrast material-enhanced (DSC) magnetic resonance (MR) imaging performed after external beam radiation therapy (EBRT) can be used to distinguish recurrent glioblastoma multiforme (GBM) from radiation necrosis. Fifty-seven patients were enrolled in this HIPAA-compliant institutional review board-approved retrospective study after they received a diagnosis of GBM, underwent EBRT, and were examined with DSC MR imaging, which revealed progressive contrast enhancement within the radiation field. A definitive diagnosis was established at subsequent surgical resection or clinicoradiologic follow-up. Regions of interest were retrospectively drawn around the entire contrast-enhanced region. This created T2-weighted signal intensity-time curves that produced three cerebral hemodynamic MR imaging measurements: CBV, PH, and PSR. Welch t tests were used to compare measurements between groups. Mean, maximum, and minimum relative PH and relative CBV were significantly higher (P < .01) in patients with recurrent GBM than in patients with radiation necrosis. Mean, maximum, and minimum relative PSR values were significantly lower (P < .05) in patients with recurrent GBM than in patients with radiation necrosis. These findings suggest that DSC perfusion MR imaging may be used to differentiate recurrent GBM from EBRT-induced radiation necrosis. (c) RSNA, 2009.
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                Author and article information

                Contributors
                +31-50-3612400 , +31-50-3611707 , a.van.der.hoorn@umcg.nl
                Journal
                Clin Neuroradiol
                Clin Neuroradiol
                Clinical Neuroradiology
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                1869-1439
                1869-1447
                2 May 2017
                2 May 2017
                2018
                : 28
                : 3
                : 401-411
                Affiliations
                [1 ]ISNI 0000 0004 0407 1981, GRID grid.4830.f, University Medical Center Groningen, Department of Radiology, , University of Groningen, ; Hanzeplein 1, 30.001, 9700 RB Groningen, The Netherlands
                [2 ]ISNI 0000 0004 0407 1981, GRID grid.4830.f, University Medical Center Groningen, Center for Medical Imaging-North East Netherlands, , University of Groningen, ; Groningen, The Netherlands
                [3 ]ISNI 0000 0004 0407 1981, GRID grid.4830.f, University Medical Center Groningen, Department of General Practice, , University of Groningen, ; Groningen, The Netherlands
                Author information
                http://orcid.org/0000-0003-4649-327X
                Article
                584
                10.1007/s00062-017-0584-x
                6105173
                28466127
                e2890554-da12-4316-b0d0-a322c300a5d5
                © The Author(s) 2017

                Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

                History
                : 16 December 2016
                : 4 April 2017
                Funding
                Funded by: University Medical Center Groningen (UMCG)
                Categories
                Original Article
                Custom metadata
                © Springer-Verlag GmbH Germany, part of Springer Nature 2018

                Radiology & Imaging
                treatment response assessment,meta-analysis,pseudoprogression,incidence,high-grade gliomas

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