Advances in Research on Human Meningiomas

A special issue of Cancers (ISSN 2072-6694). This special issue belongs to the section "Cancer Biomarkers".

Deadline for manuscript submissions: closed (1 July 2021) | Viewed by 23517

Special Issue Editors

1. Department of Clinical and Molecular Medicine, Faculty of Medicine and Health Sciences, Norwegian University of Science and Technology (NTNU), 7491 Trondheim, Norway
2. Department of Pathology, St. Olavs Hospital, 7006 Trondheim, Norway
Interests: brain tumours; neuropathology; Immunohistochemistry
Department of Pathology, Righospitalet, Copenhagen University Hospital. Frederik Vs vej 11, 2100 Copenhagen, Denmark
Interests: biomarkers in CNS tumors; molecular pathology

Special Issue Information

Dear Colleagues,

This Special Issue deals with human meningiomas, which are mostly benign and slow-growing tumors. Their biology can, however, be capricious as some cases recur despite a benign histology. Thus, the histopathological grading system of these tumors is suboptimal, and more objective diagnostic and prognostic biomarkers are required. For instance, methylation-based tumor classification is highly relevant. For most meningioma patients treated with optimal surgical and radiation approaches, outcomes are good. Unfortunately, some of these tumors cannot be totally resected, and some may recur even after complete resection and radiotherapy. Furthermore, both surgery and radiotherapy may have troublesome and serious complications. Accordingly, this Special Issue welcomes papers on biomarkers that can improve our diagnostic and prognostic work-up of these tumors.

Prof. Dr. Sverre Helge Torp
Dr. David Scheie
Guest Editors

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Keywords

  • meningiomas
  • biomarkers
  • immunohistochemistry
  • molecular genetics
  • diagnosis
  • prognosis

Published Papers (11 papers)

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Editorial

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2 pages, 146 KiB  
Editorial
Advances in Research on Human Meningiomas
by Sverre Helge Torp and David Scheie
Cancers 2020, 12(9), 2702; https://0-doi-org.brum.beds.ac.uk/10.3390/cancers12092702 - 21 Sep 2020
Cited by 1 | Viewed by 1272
Abstract
Meningiomas are the most common intracranial tumours in humans, constituting more than one third [...] Full article
(This article belongs to the Special Issue Advances in Research on Human Meningiomas)

Research

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13 pages, 2572 KiB  
Article
Somatostatin Receptors in Human Meningiomas—Clinicopathological Aspects
by Sofie Eline Tollefsen, Anders H. Jarmund, Borgny Ytterhus, Øyvind Salvesen, Patricia Mjønes and Sverre Helge Torp
Cancers 2021, 13(22), 5704; https://0-doi-org.brum.beds.ac.uk/10.3390/cancers13225704 - 15 Nov 2021
Cited by 3 | Viewed by 2549
Abstract
Meningiomas have high recurrence rates despite frequently benign histopathological appearances. Somatostatin receptors (SSTRs) may be reliable biomarkers that could identify patients with increased risk of recurrence. Even though SSTRs are previously detected in meningiomas, their associations to clinicopathological features remain unclear. The aim [...] Read more.
Meningiomas have high recurrence rates despite frequently benign histopathological appearances. Somatostatin receptors (SSTRs) may be reliable biomarkers that could identify patients with increased risk of recurrence. Even though SSTRs are previously detected in meningiomas, their associations to clinicopathological features remain unclear. The aim of this study was to investigate the diagnostic and prognostic value of SSTRs in a large series of human meningiomas with long follow-up data. Immunohistochemistry was used to measure the expression of SSTR1-SSTR5 in tissue samples from 162 patients diagnosed with intracranial meningiomas of World Health Organization (WHO) grade 1 or 2. Digital scoring and a manual staining index were applied to assess immunoreactivity. All SSTRs, except SSTR4, were upregulated in our series of meningiomas. SSTR1 (p = 0.036), SSTR2 (p = 0.036) and SSTR5 (p = 0.029) were associated with a higher malignancy grade. SSTR2 presented as the most reliable marker. Only SSTR2 was associated with time to recurrence (TTR) in univariate Cox regression analyses. Manual staining index was strongly correlated with digital scoring for all SSTRs (r > 0.65, p < 0.001). SSTRs, and especially SSTR2, are useful in the diagnostics of meningiomas, even though their prognostic value appears limited. Digital scoring is valuable to ensure reproducibility. Full article
(This article belongs to the Special Issue Advances in Research on Human Meningiomas)
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13 pages, 8262 KiB  
Article
Pathologic Characteristics of Pregnancy-Related Meningiomas
by Laura Giraldi, Emma Kofoed Lauridsen, Andrea Daniela Maier, Jørgen Vinsløv Hansen, Helle Broholm, Kåre Fugleholm, David Scheie and Tina Nørgaard Munch
Cancers 2021, 13(15), 3879; https://0-doi-org.brum.beds.ac.uk/10.3390/cancers13153879 - 01 Aug 2021
Cited by 6 | Viewed by 2415
Abstract
Meningiomas are the most common intracranial tumor. During pregnancy, explosive growth of a known meningioma occasionally occurs, but the underlying reasons remain unknown. Prolactin has been suggested as a possible key contributor to pregnancy-related meningioma growth. This study sets out to investigate prolactin [...] Read more.
Meningiomas are the most common intracranial tumor. During pregnancy, explosive growth of a known meningioma occasionally occurs, but the underlying reasons remain unknown. Prolactin has been suggested as a possible key contributor to pregnancy-related meningioma growth. This study sets out to investigate prolactin and prolactin receptor status in 29 patients with pregnancy-related meningiomas in Denmark, from January 1972 to December 2016, as compared to 68 controls aged 20–45 years, also undergoing resection of a meningioma. Furthermore, we investigated potential differences in the progesterone and estrogen receptor statuses, WHO grade, Ki-67 labeling indices, and locations of the resected meningiomas between the cases and controls. Immunohistochemical analyses were performed, and histopathology and intracranial location were assessed with the investigator blinded for the case–control status. None of the samples stained positive for prolactin and very few samples stained positive for prolactin receptors, equally distributed among cases and controls. Estrogen and progesterone receptors generally followed the same distributional pattern between groups, whereas above cut-point Ki-67 labeling indices for both groups were observed. In conclusion, our results did not support the notion of prolactin as a key contributor to pregnancy-related meningioma growth. Rather, the similarities between the cases and controls suggest that meningiomas early in life may comprise a distinct biological entity. Full article
(This article belongs to the Special Issue Advances in Research on Human Meningiomas)
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16 pages, 7575 KiB  
Article
FORGE: A Novel Scoring System to Predict the MIB-1 Labeling Index in Intracranial Meningiomas
by Johannes Wach, Tim Lampmann, Ági Güresir, Patrick Schuss, Hartmut Vatter, Ulrich Herrlinger, Albert Becker, Michael Hölzel, Marieta Toma and Erdem Güresir
Cancers 2021, 13(14), 3643; https://0-doi-org.brum.beds.ac.uk/10.3390/cancers13143643 - 20 Jul 2021
Cited by 10 | Viewed by 2331
Abstract
The MIB-1 index is an essential predictor of progression-free-survival (PFS) in meningioma. To date, the MIB-1 index is not available in preoperative treatment planning. A preoperative score estimating the MIB-1 index in patients with intracranial meningiomas has not been investigated so far. Between [...] Read more.
The MIB-1 index is an essential predictor of progression-free-survival (PFS) in meningioma. To date, the MIB-1 index is not available in preoperative treatment planning. A preoperative score estimating the MIB-1 index in patients with intracranial meningiomas has not been investigated so far. Between 2013 and 2019, 208 patients with tumor morphology data, MIB-1 index data, and plasma fibrinogen and serum C-reactive protein (CRP) data underwent surgery for intracranial WHO grade I and II meningioma. An optimal MIB-1 index cut-off value (≥6/<6) in the prediction of recurrence was determined by ROC curve analysis (AUC: 0.71; 95% CI: 0.55–0.87). A high MIB-1 index (≥6%) was present in 50 cases (24.0%) and was significantly associated with male sex, peritumoral edema, low baseline CRP, and low fibrinogen level in the multivariate analysis. A scoring system (“FORGE”) based on sex, peritumoral edema, preoperative CRP value, and plasma fibrinogen level supports prediction of the MIB-1 index (sensitivity 62%, specificity 79%). The MIB-1 labeling index and the FORGE score are significantly associated with an increased risk of poor PFS time. We suggest a novel score (“FORGE”) to preoperatively estimate the risk of an increased MIB-1 index (≥6%), which might help in surgical decision making and follow-up interval determination and inform future trials investigating inflammatory burden and proliferative activity. Full article
(This article belongs to the Special Issue Advances in Research on Human Meningiomas)
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14 pages, 9396 KiB  
Article
Predictors of Survival in Atypical Meningiomas
by Michele Da Broi, Paola Borrelli and Torstein R. Meling
Cancers 2021, 13(8), 1970; https://0-doi-org.brum.beds.ac.uk/10.3390/cancers13081970 - 21 Apr 2021
Cited by 7 | Viewed by 1829
Abstract
Introduction: Predictors of survival and progression of disease in atypical meningiomas are less well documented in the literature compared to benign meningiomas. Higher grade meningiomas tend to recur often and one of the most critical aspects is how to best deal with relapses. [...] Read more.
Introduction: Predictors of survival and progression of disease in atypical meningiomas are less well documented in the literature compared to benign meningiomas. Higher grade meningiomas tend to recur often and one of the most critical aspects is how to best deal with relapses. Methods: A total of 77 consecutive patients who underwent craniotomy for atypical meningioma between 1990–2010 at Oslo University Hospital (OUH) were reviewed. Results: Median age at surgery was 62.21 [interquartile range (IQR): 22.87] years. Fifty-one patients (66.2%) had neurological deficits at presentation. Fifty-four patients (70.1%) underwent gross total resection (GTR). Thirty-nine patients (50.7%) had improved/stable neurological outcomes at 6–12 months. Twenty-two patients (28.6%) underwent retreatment, of whom 20 (26.0%) were subjected to resection followed by adjuvant radiotherapy. Overall survival (OS) was significantly longer in patients <65 years (p < 0.001), with preoperative Karnofsky performance scale (KPS) score of ≥ 70 (p = 0.006), and who required no retreatment (p = 0.033). GTR significantly prolonged the retreatment-free survival rate (p < 0.001). STR carried almost a six-fold greater risk of neurological outcome deterioration (p = 0.044). Conclusions: GTR significantly prolonged retreatment-free survival but had no significant impact on OS. STR was a significant risk factor for deteriorated neurological outcome. Age, preoperative KPS, and retreatment were all strong predictors of OS. Median time-to-retreatment (TTR) did not shorten significantly throughout repeated surgeries. Full article
(This article belongs to the Special Issue Advances in Research on Human Meningiomas)
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23 pages, 4273 KiB  
Article
Are We Benign? What Can Wnt Signaling Pathway and Epithelial to Mesenchymal Transition Tell Us about Intracranial Meningioma Progression
by Anja Bukovac, Anja Kafka, Marina Raguž, Petar Brlek, Katarina Dragičević, Danko Müller and Nives Pećina-Šlaus
Cancers 2021, 13(7), 1633; https://0-doi-org.brum.beds.ac.uk/10.3390/cancers13071633 - 01 Apr 2021
Cited by 12 | Viewed by 2513
Abstract
Epithelial to mesenchymal transition (EMT), which is characterized by the reduced expression of E-cadherin and increased expression of N-cadherin, plays an important role in the tumor invasion and metastasis. Classical Wnt signaling pathway has a tight link with EMT and it has been [...] Read more.
Epithelial to mesenchymal transition (EMT), which is characterized by the reduced expression of E-cadherin and increased expression of N-cadherin, plays an important role in the tumor invasion and metastasis. Classical Wnt signaling pathway has a tight link with EMT and it has been shown that nuclear translocation of β-catenin can induce EMT. This research has showed that genes that are involved in cadherin switch, CDH1 and CDH2, play a role in meningioma progression. Increased N-cadherin expression in relation to E-cadherin was recorded. In meningioma, transcription factors SNAIL, SLUG, and TWIST1 demonstrated strong expression in relation to E- and N-cadherin. The expression of SNAIL and SLUG was significantly associated with higher grades (p = 0.001), indicating their role in meningioma progression. Higher grades also recorded an increased expression of total β-catenin followed by an increased expression of its active form (p = 0.000). This research brings the results of genetic and protein analyzes of important molecules that are involved in Wnt and EMT signaling pathways and reveals their role in intracranial meningioma. The results of this study offer guidelines and new markers of progression for future research and reveal new molecular targets of therapeutic interventions. Full article
(This article belongs to the Special Issue Advances in Research on Human Meningiomas)
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12 pages, 840 KiB  
Article
Predictors of Survival in Subtotally Resected WHO Grade I Skull Base Meningiomas
by Michele Da Broi, Paola Borrelli and Torstein R. Meling
Cancers 2021, 13(6), 1451; https://0-doi-org.brum.beds.ac.uk/10.3390/cancers13061451 - 22 Mar 2021
Cited by 5 | Viewed by 1685
Abstract
Background: Although gross total resection (GTR) is the goal in meningioma surgery, this can sometimes be difficult to achieve in skull base meningiomas. We analyzed clinical outcomes and predictors of survival for subtotally resected benign meningiomas. Methods: A total of 212 consecutive patients [...] Read more.
Background: Although gross total resection (GTR) is the goal in meningioma surgery, this can sometimes be difficult to achieve in skull base meningiomas. We analyzed clinical outcomes and predictors of survival for subtotally resected benign meningiomas. Methods: A total of 212 consecutive patients who underwent subtotal resection (STR) for benign skull base meningioma between 1990–2010 were investigated. Results: Median age was 57.7 [IQR 18.8] years, median preoperative Karnofsky performance status (KPS) was 80.0 [IQR 20.0], 75 patients (35.4%) had posterior fossa meningioma. After a median follow-up of 6.2 [IQR 7.9] years, retreatment (either radiotherapy or repeated surgery) rate was 16% at 1-year, 27% at 3-years, 34% at 5-years, and 38% at 10-years. Ten patients (4.7%) died perioperatively, 9 (3.5%) had postoperative hematomas, and 2 (0.8%) had postoperative infections. Neurological outcome at final visit was improved/stable in 122 patients (70%). Multivariable analysis identified advanced age and preoperative KPS < 70 as negative predictors for overall survival (OS). Patients who underwent retreatment had no significant reduction of OS. Conclusions: Advanced age and preoperative KPS were independent predictors of OS. Retreatments did not prolong nor shorten the OS. Clinical outcomes in STR skull base meningiomas were generally worse compared to cohorts with high rates of GTR. Full article
(This article belongs to the Special Issue Advances in Research on Human Meningiomas)
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13 pages, 1190 KiB  
Article
The Prognostic Value of Methylation Signatures and NF2 Mutations in Atypical Meningiomas
by Rahmina Meta, Henning B. Boldt, Bjarne W. Kristensen, Felix Sahm, Wenche Sjursen and Sverre H. Torp
Cancers 2021, 13(6), 1262; https://0-doi-org.brum.beds.ac.uk/10.3390/cancers13061262 - 12 Mar 2021
Cited by 5 | Viewed by 2122
Abstract
Background: Due to the solely subjective histopathological assessment, the WHO 2016 classification of human meningiomas is subject to interobserver variation. Consequently, the need for more reliable and objective markers are highly needed. The aim of this pilot study was to apply genome-wide [...] Read more.
Background: Due to the solely subjective histopathological assessment, the WHO 2016 classification of human meningiomas is subject to interobserver variation. Consequently, the need for more reliable and objective markers are highly needed. The aim of this pilot study was to apply genome-wide DNA methylation analysis on a series of atypical meningiomas to evaluate the practical utility of this approach, examine whether prognostic subclasses are achieved and investigate whether there is an association between the methylation subclasses with poor prognosis and time to recurrence. NF1/2 mutation analyses were also performed to explore the prognostic value of such mutations in these atypical meningiomas. Methods: Twenty intracranial WHO grade II atypical meningiomas from adult patients were included. They consisted of 10 cases with recurrence (group I), and 10 cases without recurrence (group II). The formalin-fixed and paraffin-embedded tissues underwent standardized genome-wide DNA methylation analysis, and the profiles were matched with the reference library and tumor classifier from Heidelberg. NF1/2 somatic mutation analyses were performed using the CNSv1panel from Düsseldorf. Results: Eighteen out of 20 cases matched to the meningioma class using the common brain tumor classifier (v11b4). Four of these cases matched to a methylation subclass related to a prognostic subgroup based on a cut-off of 0.9. NF2 mutations were detected in 55% of cases across both groups, and the most prominent copy number alterations were chromosomal losses of 22q, 1p and 14q. No significant NF1 mutations were identified. Conclusions: Genome-wide DNA methylation profiling represents a useful tool in the diagnostics of meningiomas, however, methodological adjustments need to be addressed. Full article
(This article belongs to the Special Issue Advances in Research on Human Meningiomas)
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8 pages, 245 KiB  
Article
Prognostic Factors for Functional Outcome of Patients with Optic Nerve Sheath Meningiomas Treated with Stereotactic Radiotherapy–Evaluation of Own and Meta-Analysis of Published Data
by Bogdan Pintea, Azize Boström, Sotiris Katsigiannis, Konstantinos Gousias, Rares Pintea, Brigitta Baumert and Jan Boström
Cancers 2021, 13(3), 522; https://0-doi-org.brum.beds.ac.uk/10.3390/cancers13030522 - 29 Jan 2021
Cited by 4 | Viewed by 1754
Abstract
Objective: To evaluate prognostic factors for a favorable outcome (improvement of the visual acuity or visual fields) after fractionated stereotactic radiotherapy (fSRT) of optic nerve sheath meningioma (ONSM). Methods: We performed a database search for ONSM treatments during the period from April 2008 [...] Read more.
Objective: To evaluate prognostic factors for a favorable outcome (improvement of the visual acuity or visual fields) after fractionated stereotactic radiotherapy (fSRT) of optic nerve sheath meningioma (ONSM). Methods: We performed a database search for ONSM treatments during the period from April 2008 to September 2019 in the prospective database for stereotactic radiosurgery/radiotherapy (SRS/SRT) of the Robert Janker Clinic Bonn (Department of Radiotherapy) and performed a literature review and meta-analysis of published data on ONSM between 2010 and 2019. Ophthalmic status before and after treatment was evaluated and the collective was dichotomized into two groups: functional improvement (FI; improvement of either visual acuity or visual fields) and non functional improvement (NFI; with stable or deteriorating visual acuity or visual fields). The two groups were compared regarding different variables: pretreatment visual acuity, age, gender, gross tumor volume (GTV), follow up (FU) time, tumor localization, and maximal retina dose. Results: Overall, 13 stereotactic radiotherapies were performed for ONSM (12 × fSRT, 1 × SRS). Mean follow up was 3 years (range: 1–5 years). The total dose was 50.4 Gy (5 × 1.8 Gy/week) in 12 patients treated with fSRT and 1 × 14 Gy in one SRS case. Mean GTV was 1.13 ccm (range: 0.44–2.20 ccm). During follow up, all tumors were stable or showed shrinkage of tumor volume (100% tumor control), no adverse events were observed, 53% of the patients achieved either better visual acuity or visual fields. Pretreatment visual acuity was significantly different between the FI and the NFI group (0.17 vs. 0.63, p = 0.03) in our series and in the meta analysis (p < 0.01). Moreover, shorter FU time and lower retinal dose were significantly linked (p < 0.05 and p < 0.01, respectively) with a better outcome in the meta-analysis but not in our patient cohort. Intracranial tumor localization, gender, and age were not significantly different between the two outcome groups. Conclusion: FSRT for ONSM achieves in over 50% of cases an improvement of the ophthalmic status with low morbidity and excellent tumor control in our series and the meta analysis. Patients with a favorable outcome had in all analysis a significantly higher visual acuity before treatment start. Therefore, we advocate using fSRT as early as possible before vision deterioration occurs. Full article
(This article belongs to the Special Issue Advances in Research on Human Meningiomas)
10 pages, 14331 KiB  
Article
Mitotic and Proliferative Indices in WHO Grade III Meningioma
by Andrea Daniela Maier, Christian Beltoft Brøchner, Jiri Bartek Jr., Frank Eriksson, Heidi Ugleholdt, Helle Broholm and Tiit Mathiesen
Cancers 2020, 12(11), 3351; https://0-doi-org.brum.beds.ac.uk/10.3390/cancers12113351 - 12 Nov 2020
Cited by 7 | Viewed by 2032
Abstract
Meningiomas with inherently high mitotic indices and poor prognosis, such as WHO grade III meningiomas, have not been investigated separately to establish interchangeability between conventional mitotic index counted on H&E stained slides (MI) and mitotic index counted on phosphohistone-H3 stained slides (PHH3 MI). [...] Read more.
Meningiomas with inherently high mitotic indices and poor prognosis, such as WHO grade III meningiomas, have not been investigated separately to establish interchangeability between conventional mitotic index counted on H&E stained slides (MI) and mitotic index counted on phosphohistone-H3 stained slides (PHH3 MI). This study investigates the agreement of MI and PHH3 MI and to analyze the association of progression-free survival (PFS) and MI, PHH3 MI, and the proliferative index (PI, Ki-67) in WHO grade III meningioma. Tumor specimens from 24 consecutive patients were analyzed for expression of Ki-67, PHH3 MI, and MI. Quantification was performed independently by two observers who made replicate counts in hot spots and overall tumor staining. Repeatability in replicate counts from MI and PHH3 MI was low in both observers. Consequently, we could not report the agreement. MI, PHH3 MI and hot spot counts of Ki-67 were associated with PFS (MI hot spot HR = 1.61, 95% CI 1.12–2.31, p = 0.010; PHH3 MI hot spot HR = 1.59, 95% CI 1.15–2.21, p = 0.006; Ki-67 hot spot HR = 1.06, 95% CI 1.02–1.11. p = 0.004). We found markedly low repeatability of manually counted MI and PHH3 MI in WHO grade III meningioma, and we could not conclude that the two methods agreed. Subsequently, quantification with better repeatability should be sought. All three biomarkers were associated with PFS. Full article
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Other

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11 pages, 432 KiB  
Systematic Review
Meningiomas and Cognitive Impairment after Treatment: A Systematic and Narrative Review
by Renato Gondar, Gildas Patet, Karl Schaller and Torstein R. Meling
Cancers 2021, 13(8), 1846; https://0-doi-org.brum.beds.ac.uk/10.3390/cancers13081846 - 13 Apr 2021
Cited by 10 | Viewed by 2081
Abstract
Clinical outcomes after surgery for intracranial meningiomas might be overvalued as cognitive dimensions and quality of life are probably underreported. This review aims to summarize the current state of cognitive screening and treatment-related outcomes after meningioma surgery. We present a systematic review (Preferred [...] Read more.
Clinical outcomes after surgery for intracranial meningiomas might be overvalued as cognitive dimensions and quality of life are probably underreported. This review aims to summarize the current state of cognitive screening and treatment-related outcomes after meningioma surgery. We present a systematic review (Preferred Reporting Items for Systematic reviews and Meta-Analyses (PRISMA-P) 2015-based) of cognitive outcomes after intracranial meningioma surgery. A total of 1572 patients (range 9–261) with a mean age of 58.4 years (range 23–87), and predominantly female (n = 1084, 68.9%) were identified. Mean follow-up time after treatment was 0.86 ± 0.3 years. Neuropsychological assessment was very heterogeneous, but five dimensions of cognition were described: memory (19/22); attention (18/22); executive functions (17/22); language (11/22); flexibility (11/22 studies). Cognitive abilities were impaired in 18 studies (81.8%), but only 1 showed deterioration in all dimensions simultaneously. Memory was the most affected. with significant post-therapy impairment in 9 studies (40.9%). Postoperatively, only 4 studies (18.2%) showed improvement in at least one dimension. Meningioma patients had significantly lower cognitive scores when compared to healthy subjects. Surgery and radiotherapy for meningiomas were associated with cognitive impairment, probably followed by a partial recovery. Cognition is poorly defined, and the assessment tools employed lack standardization. Cognitive impairment is probably underreported in meningioma patients. Full article
(This article belongs to the Special Issue Advances in Research on Human Meningiomas)
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