Impact of vascular supply variability on the prognosis of meningioma patients: a retrospective study based on territory arterial spin labeling

Introduction

Meningiomas represent the most common intracranial tumor, which are classified into grade 1, 2 and 3 according to updated World Health Organization (WHO) classification of tumors of the nervous system (1). Despite generally favorable functional recovery through surgery or radiotherapy, the recurrence rates per 100-person-year for WHO grade 1 meningiomas vary from 0.00 to 2.36, while rates for WHO grade 2 meningiomas range from 7.35 to 11.46, with a non-negligible possibility of mortality. Survival rates for WHO grade 3 meningiomas have been reported to be as low as 8.3% at 5 years, posing challenges in obtaining long-term recurrence rate data (2-4). Several studies have discussed the prognostic factors of meningioma including demographic and tumor-specific variables; however, all these mentioned factors are insufficient to reflect the tumor’s behavior and clinical outcome reliably, which indicates that other main factors influencing prognosis may have not been identified clearly, complicating pre-treatment prognostic assessment.

Understanding the vascular supply of meningiomas is critical to clinical treatment. Raper and colleagues (5) have suggested that embolization-related complications, such as ischemic, are more probable when the tumor is supplied by a targeted artery. In cases where the lesion receives blood supply from the internal carotid artery (ICA), pre-embolization aiming at reducing tumor size and hemorrhagic risk may inadvertently compromise cerebral cortical or neural function, potentially leading to blindness, paralysis, or sensory deficits (6,7). While the impact of meningiomas with different feeders on the treatment options has been studied frequently, the impact of feeding vasculatures on prognosis has scarcely been investigated. Prior investigations indicate a correlation between higher-grade meningiomas and ICA supply, suggesting a potential association between vascular origin and both prognosis and clinical presentation (8,9). This warrants further investigation into the association between vascular supply and prognostic outcomes.

The clinical gold standard for assessing tumor vascularity is digital subtraction angiography (DSA); however, it is an invasive, radioactive, and costly procedure. Magnetic resonance (MR) perfusion-weighted imaging encompasses dynamic susceptibility contrast magnetic resonance imaging (MRI), dynamic contrast-enhanced MRI, and arterial spin labeling techniques. Notably, arterial spin labeling enables noninvasive assessment of tissue blood perfusion without the administration of contrast agents (10). Territorial arterial spin labelling (t-ASL) is a non-invasive MRI technique that quantitatively measures cerebral blood perfusion without the need for contrast agents. It utilizes endogenous blood protons as an intrinsic tracer. Several studies have demonstrated good agreement between the identification of feeding artery origins on t-ASL and DSA results (11-13). As a non-invasive, contrast-free technique, t-ASL enables the visualization of cerebral perfusion in specific regions and delineation of arterial territories (14,15). The findings from our previous research have demonstrated the successful depiction of meningioma blood supply using t-ASL, providing radiologists with easily interpretable results (16). In that study, we found that ICA-supplied meningiomas were more likely to demonstrate motor and sense dysfunction, meanwhile, and atypical meningiomas were all supplied by ICA, indicating possible relationships between blood supply, clinical manifestation and pathology. Consequently, this study aims to ascertain whether the variations in perfusion, as revealed by t-ASL, can influence the clinical symptoms, short-term and long-term outcome in meningioma patients by exploring the relationship between t-ASL based perfusion characteristics with patient demographics, tumor characteristics, Simpson grade of surgical resection, immunohistochemical parameters and postoperative pathological grade of meningiomas. We present this article in accordance with the STROBE reporting checklist (available at https://qims.amegroups.com/article/view/10.21037/qims-24-1010/rc).

Methods

Patients

The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and received approval from the institutional board and ethical committee of Huashan Hospital, Fudan University (No. KY2022-691), with all written informed consents being waived due to the retrospective nature of the study. A total of 51 patients were included in our study between November 2018 and December 2019. The inclusion criteria were as follows: (I) pathological diagnosis of meningioma; (II) preoperative t-ASL imaging; (III) uniform surgical treatment by our institutional team and pathological confirmation of meningioma; (IV) complete preoperative and postoperative Glasgow Coma Score (GCS), pre-operational and 3-year post-discharge Karnofsky Performance Score (KPS) data. The exclusion criteria were as follows: (I) t-ASL images with artifacts (n=6); (II) non-meningioma pathological diagnoses (n=4); (III) incomplete clinical data or loss to follow-up (n=8). The enrollment of our study comprised a total of 33 patients. Details of GCS (17) and KPS (18) are presented in Table S1.

Image acquisition

For conventional MR imaging, the MR imaging studies were performed on a 3.0 T scanner equipped with a 32-channel receiver head coil array. Following sequences were acquired: axial pre-contrast T1-weighted images [repetition time (TR)/echo time (TE) =2,000/18 ms, matrix =358×512, field of view (FOV) =240×240 mm², bandwidth =122 Hz/pixel, slice thickness/gap =3/0 mm, number of excitations (NEX) =1]; axial T2-weighted fluid attenuated inversion recovery (FLAIR) images (TR/TE =4,000/94 ms, matrix =314×512, FOV =240×240 mm², bandwidth =122 Hz/pixel, slice thickness/gap =3/0 mm, NEX =2); 3-dimensional time-of-flight magnetic resonance angiography (3D-TOF-MRA), TR/TE =8.2/3.2 ms, matrix =320×320, flip angle =12°, FOV =240×240 mm², slice thickness =1 mm); contrast-enhanced T1-weighted images were obtained after bolus injection of gadolinium-diethylenetriaminepentaacetic acid (Gd-DTPA) 20 mL, with a dose of 0.1 mmol/kg (0.2 mL/kg) body weight. All axial scans were congruent to facilitate consistent comparisons.

For t-ASL, the labelling plane was identified from 3D-TOF-MRA to: (I) maximize the separation between ICA and external carotid artery (ECA) to prevent operation errors and motion artifacts; (II) ensure proximity of vertical segments of the ICA, ECA and vertebral artery (VA) to the cranium entrance. Bilateral ICAs and ECAs were individually labelled with super-selective ASL (SS-ASL) and bilateral VAs were labelled by vessel-encoded ASL (VE-ASL) for selective vessel inversion. Labelling spots, circles with 25–30 mm radius, were set at the centers of ICAs, ECAs and VAs on the selected plane. The corresponding whole-brain perfusion images were acquired (TR/TE =4,550/10.6 ms, matrix =4 arms with 514 points per arm, FOV =200×200 mm², flip angle =90°, slice thickness =4 mm, NEX =2) with adjustments made to the number of slices to completely cover the brain tissue distal to the labelling plane. The total scan time was approximately 6 minutes 59 seconds.

Post-processing and feeder identification

t-ASL images were obtained by the subtraction of label and control acquisitions. Maximum intensity projections were generated in transversal, coronal and sagittal orientation using Advantage Workstation 4.5.

Tumor perfusion maps on t-ASL were carefully analyzed to identify feeding arteries and a quantitative system was used to determine the blood feeder of meningioma (16). The evaluation was conducted on the maximum axial plane of the meningioma, containing two aspects:

• Signal intensity (SI): a difference in SI (SI_difference) is determined by comparing the meningioma area’s SI to that of a selected contralateral area using t-ASL post-processing results. SI_difference was calculated as follows:

  $$S{I}_{Difference}=\frac{S{I}_{meningioma}-S{I}_{contralateralarea}}{S{I}_{contralateralarea}}\times 100\%$$[1]

  A difference greater than 20% is considered significant.
• Area percentage:
  • For the ICA supply, meningiomas are classified based on the area with SI_difference over 20%. If this constitutes more than 90% of the meningioma area on ICA maps, it is categorized as ICA-supplied;
  • For the ECA supply, the same area threshold applies to categorize a meningioma as ECA-supplied;
  • For ICA co-supplied meningiomas, if the area with an SI_difference over 20% ranges between 50–90% on ICA maps, it’s considered co-supplied by ICA and other feeding arteries;
  • The classification of meningiomas as non-ICA co-supplied is applicable when an SI_difference on ICA maps encompasses less than 50% and on ECA maps less than 90% of the area, both exceeding a threshold of 20%.

The SI and area were calculated via ITK-SNAP software (version 3.8.0) (19). t-ASL images were independently analyzed by two experienced neuro-radiologists (one with 10 years of experience in neurological radiology and another with 18 years of experience), who were blinded to clinical histories. After recording the analysis results from each reader, the inter-observer agreement was calculated, and these two neuro-radiologists were asked to discuss and render a final judgement after negotiation (Table S2). Two illustrations (Figure S1) were provided to help understand how to evaluate the blood feeders via the above criteria interpretations.

Tumor volume measurement

A third neuroradiologist (with 20 years of experience in neurological radiology) manually delineated the regions of interest (ROIs) of the meningioma on T1-enhanced sequence at each level. The tumor volume was then computed using ITK-SNAP software, which aggregates the values of the area and slice thickness to yield the tumor’s total volume.

Clinical data recording

Clinical data for each patient, was recorded by one neurosurgeon with experience of more than 10 years, who was the first assistant during operation. Clinical parameters included the demographics, surgical findings, pathological results and clinical outcome. Dizziness of patients with meningiomas in clinical manifestations was defined as both subjective dizziness and documented previous medical records of vestibular dysfunction. The determination of other clinical manifestations was based on the admission history. Simpson grading system, as a classification method used to describe the extent of removal of a meningioma, classifies the extent of tumor resection from grade 1 (complete resection with excision of involved dura and bone) to grade 4 (simple decompression with no attempt at tumor removal) and was carefully recorded in this study. The detailed pathological results including histological diagnosis, Ki-67 index (a measurement of cell proliferation based on the presence of the Ki-67 protein in cell nuclei) and meningioma-related immunohistochemical staining were also noted.

Prognostic evaluation

The prognostic evaluation employed both GCS and the KPS. GCS, as a short-term tool, was used to assess the conscious level before and after operation in our study. KPS score of 90, which was used as a threshold to differentiate good and poor long-term outcomes in meningioma patients, was evaluated before surgery and 3 years after surgery (20). Multigroup comparison among four groups of meningiomas was described in Table S3.

Statistical analysis

Statistical analysis was performed with R software (version 4.1.2) (21). Continuous variables were presented as the mean ± standard deviation (for normal distribution) or as the median value with the 25^th and 75^th percentiles (for non-normal distribution), with normality assessed by Shapiro-Wilk test (n≤50). Categorical variables were expressed in terms of count and proportion. Analysis of variance (ANOVA) (for normal distribution) or Kruskal-Wallis test (for non-normal distribution) was applied to evaluate the groups. Chi-squared test or Fisher’s exact test was employed to compare qualitative variables.

Multiple group comparisons were adjusted for using the least significant difference (LSD) method. Correlations were established using Pearson’s coefficient for continuous variables and Spearman’s rank correlation for categorical variables, to account for linear and monotonic relationships respectively. To address multicollinearity among predictors, a Ridge regression analysis was implemented. This approach provided bias-corrected odds ratios (ORs) and coefficients, crucial for elucidating the influence of vascular supply on meningioma prognosis as determined by t-ASL. A P value less than 0.05 was indicative of statistical significance for all aforementioned tests.

Results

A total of 33 meningioma patients were finally recruited, including 8 male and 25 females, with an average age of 53.42±9.66 years. Clinical parameters of all 33 patients with meningioma are shown in Table 1. The mean volume of meningioma was 34.97±36.11 mm³, and 3 were grade 2 meningiomas, while other 30 were grade 1 meningiomas. The cohort was categorized based on the differences in vascular supply determined by t-ASL into four groups: ICA-supplied (n=7), ECA-supplied (n=10), ICA co-supplied group (n=10), and non-ICA co-supplied group (n=6). No participant exhibited a sole VA or basilar artery (BA) supply. The inter-observer reliability for these classifications was determined to be excellent (κ=0.959, Table S2).

The analysis of differences among four groups with different blood supply revealed significant difference in symptom ‘dizziness’ (P=0.003), pre-operative GCS (P=0.010), pre-operative KPS (P=0.001), post-operative GCS (P=0.029) and 3-year post-operative KPS scores (P=0.012). The ICA group’s distinct clinical profile was further emphasized by a higher prevalence of dizziness. The LSD post-hoc analysis elucidated significant disparities in clinical outcomes and symptoms among these four groups. The ICA group, in particular, exhibited lower scores in pre- and post-operative GCS and KPS score (all P<0.05, Figure 1). The detailed analytic results were showed in Table 2. These findings highlight the necessity of considering ICA-supplied meningioma in clinical assessments and treatment planning.

Figure 1 The analysis of differences in pre- and post-surgical scores among four groups with varying blood supply. The ICA group, in particular, demonstrated significantly lower scores in pre- and post-operative GCS and KPS score (all P<0.05). *, P<0.05; **, P<0.01; ***, P<0.001. GCS, Glasgow Coma Score; KPS, Karnofsky Performance Score; ICA, internal carotid artery; ECA, external carotid artery; ns, not significant.

Then we simplified our groups into exclusively ICA co-supplied group and non-ICA co-supplied group, trying to find the most relevant factors with ICA blood supply in meningiomas. The correlation analysis elucidates significant associations of ICA-supplied meningiomas with specific clinical variables, notably in male (r=0.398, P=0.022), dizziness (r=0.639, P=0.030), headache (r=−0.378, P=0.030), visual disturbance (r=0.352, P=0.045), as well as pre- and post-operative GCS and KPS scores (seen in Figure 2 and Table 3). The findings suggested that male patients with ICA-supplied meningioma were more prone to experiencing symptoms such as dizziness, headache, and visual disturbance, along with pre- and post-operative GCS and KPS scores.

Figure 2 Parameters significantly correlated with ICA-supplied meningiomas. The correlation analysis reveals significant associations between ICA-supplied meningiomas and specific clinical variables, particularly in terms of gender, dizziness, headache, visual disturbance, as well as pre- and post-operative GCS and KPS scores. ICA, internal carotid artery; KPS, Karnofsky Performance Score; GCS, Glasgow Coma Score.

A 3-year post-operative KPS score of 90 was used in further analysis as a threshold to differentiate good and poor long-term outcome in meningioma patients. Several factors exhibited significant correlations between ICA-supplied meningiomas and clinical features, including: presence of male, dizziness, visual disturbance, and both high pre- and post-operative GCS and KPS scores (Figure 3). The Ridge regression analysis was conducted to understand the impact of various factors on 3-year post-operative clinical outcome (Figure 4). Our result highlighted that pre-operative GCS score [OR: 1.566, 95% confidence interval (CI): 1.301–2.348] had a significantly positive impact on the long-term outcome of patients. In contrast, meningiomas with ICA blood supply (OR: 0.180, 95% CI: 0.078–0.605), skull-base location (OR: 0.275, 95% CI: 0.093–1.141), and pathologically-confirmed WHO grade 2 (OR: 0.172, 95% CI: 0.067–1.000) were negatively associated with favorable long-term outcome (Table 4).

Figure 3 Factors correlated significantly with post-operative 3-year KPS. The presence of dizziness, visual disturbance, skull base location, grade 1 meningioma, and both high pre- and post-operative GCS and KPS scores exhibited significant correlations with ICA-supplied meningiomas in terms of clinical features. KPS, Karnofsky Performance Score; GCS, Glasgow Coma Score; ICA, internal carotid artery.

Figure 4 Factors significantly influencing patient’s KPS score by Ridge regression analysis. The pre-operative GCS score significantly influenced the long-term prognosis of patients. Meningiomas with ICA blood supply, and pathologically-confirmed WHO grade 2 were associated with an unfavorable long-term outcome. KPS, Karnofsky Performance Score; GCS, Glasgow Coma Score; ICA, internal carotid artery; WHO, World Health Organization.

Discussion

The prognosis of meningiomas has consistently been a prominent subject of research. The analysis of the relationship between prognostic factors and various characteristics of meningiomas has been extensively studied in previous research (22-24). While numerous studies have emphasized the significance of blood perfusion in survival analysis for brain tumors, limited attention has been given to investigating the association between blood supply and prognosis of meningiomas (11,13,25,26). The findings of our investigation into the clinical information and follow-up of patients with meningiomas underscore the crucial role played by vascular supply, particularly from ICA, in influencing clinical presentations and prognosis. Distinctive features of meningiomas with blood supply from ICA were elucidated: ICA-supplied meningiomas tended to be located deeper than other types, exhibiting dizziness and visual disturbance, and exerted a negative impact on both short-term and long-term outcomes.

The vascular supply to meningiomas, primarily derived from the internal and ECA systems, plays a pivotal role in surgical intervention. The ICA-derived feeding arteries, chiefly the tentorial artery, dorsal meningeal artery, and posterior ethmoidal artery, and the ECA-derived feeders, mainly the middle meningeal artery, are not only responsible for blood supply but also serve as an attachment point for anchoring the tumor to the dura mater (27). Previous research indicated that meningiomas with pial feeders originating from the ICA are prone to tumor-brain adhesion, which complicated surgical removal compared to those with dural feeders originating from ECA (28). Similar findings was proposed by Pistolesi et al. as well, who linked peritumoral edema with pial blood supply, emphasizing its role in increasing surgical complexity and deteriorating prognosis (8). The collective findings from these prior studies, in conjunction with our results, suggested that the prognosis for meningiomas supplied by ICA may be compromised attributed to the heightened intricacy of surgical intervention. Consequently, preoperative knowledge of the tumor’s vascular supply can provide a preliminary prognostic assessment.

Clinically, our study identified a higher prevalence (71.43%) of dizziness in patients with meningiomas supplied by ICA, which commonly associated with benign paroxysmal positional vertigo (BPPV) and peripheral vertigo, often resulting from ischemia in the vertebral basilar system (Table 2). Subclavian steal syndrome is caused by atherosclerotic stenosis or occlusion of the subclavian artery or the proximal end of the brachiocephalic trunk. This leads to retrograde blood flow from the ipsilateral VA into the distal end of the subclavian artery, supplying blood to the affected upper limb and causing brain ischemia, particularly in the brain stem. We hypothesize that this dizziness may indicate ischemic changes due to the “blood-stealing” phenomenon from BA system (especially the anterior-inferior cerebellar artery, which supplies the inner ear) to ICA supplied region (29,30). Therefore, we believe that it is imperative to further investigate whether the occurrence of dizziness in the ICA group can be attributed to alterations in perfusion when compared with other groups devoid of such symptoms. Meanwhile, an alternative explanation for the dizziness observed in ICA-supplied meningiomas was related to the suppression of certain brain regions. Previous research showed that the stimulation of the inferior vestibular could result in dizziness (31). The primary complaint in cases supplied by ECA was headache. In this study, as the tumors supplied by ECA were predominantly located on the convex surface of the brain (70%, 7/10), which may exert traction and pressure on endocranial structures. Moreover, the tumor is prone to grow, infiltrate, and adhere with the local dura mater. As a result, it directly stimulates the nerves within the dura mater and subsequently causes headaches (32). This symptomatology could potentially serve as a preliminary indicator of the meningioma’s blood supply.

Furthermore, other clinical features correlated significantly with blood supply, including gender. This observed correlation with male gender (r=0.398, P=0.022) may potentially reflect hormonal influences on vascularization. Although pathological grade was closely related to patient’s clinical outcome, no significant relation (r=0.09, P>0.69) was found between WHO grade and ICA/ECA blood supply, which was contradictory to our prior findings (16). In Ridge regression analysis of our study, skull-base location (OR: 0.275, 95% CI: 0.093–1.141) revealed none significant association with long-term outcome. A larger cohort was necessitated to investigate the relationship between blood supply and tumor malignancy and skull-base location in meningiomas.

Our study is constrained by certain limitations. Firstly, this study is a single-center retrospective study with a limited sample size and restricted representation of the male population, thus potentially introducing selection bias and lacking external validation. There were no WHO grade 3 meningiomas in this study, and only three cases of WHO grade 2 meningiomas were identified. The findings derived from this study can be extrapolated to encompass the majority of WHO grade 1 meningiomas. Secondly, the assessment of blood supply by t-ASL was mainly based on the hyper-perfusion of tumor, while hypo-perfused meningiomas were not taken into consideration. The skull-base meningiomas may require a larger cohort for investigation. Additionally, while the evaluation of prognosis was primarily based on KPS, the presence of recurrence or tumor growth is also important and warrants further discussion.

Conclusions

Our study demonstrates that the vascular supply, particularly from ICA, affects both the clinical manifestations and outcomes of meningioma patients. Dizziness and headache may be the distinctive symptoms in meningioma patients supplied by ICA and ECA. Meningiomas involving ICA supply, and with a high WHO grade may have unfavorable prognosis.

Acknowledgments

Funding: The work was supported by “Science and Technology Innovation Action Plan” of Shanghai Science and Technology Commission (grant No. 22S31905900).

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://qims.amegroups.com/article/view/10.21037/qims-24-1010/rc

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://qims.amegroups.com/article/view/10.21037/qims-24-1010/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are 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. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013) and received approval from the institutional board and ethical committee of Huashan Hospital, Fudan University (No. KY2022-691), with the requirement of written informed consent being waived due to the retrospective nature of the study.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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