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The Predictive Value of Conventional Magnetic Resonance Imaging Sequences on Operative Findings and Histopathology of Intracranial Meningiomas: A Prospective Study
Correspondence Address: Source of Support: None, Conflict of Interest: None DOI: 10.4103/0028-3886.273632
Keywords: Fluid attenuated inversion recovery, histopathology, magnetic resonance imaging, meningioma, meningioma–brain interface, operative plane
Intracranial meningiomas, in general, are benign, extra-axial, encapsulated tumors that when totally excised have a good outcome. However, some patients experience postoperative morbidity and recurrence depending on the tumor location, size, extent into anatomically significant areas, histological grade, and completeness of excision.[1],[2],[3],[4],[5],[6],[7],[8],[9],[10],[11],[12],[13] There are several aspects in a meningioma surgery that affect the operative technique and extent of resection.[1],[3],[4],[11],[13],[14],[15],[16] The tumor consistency, its vascularization, and surgical plane are some of the important determinants. These considerations become important, especially in skull base meningiomas and in those that involve adjacent neurovascular structures.[1],[2],[3],[4],[11],[13] For instance, surgical morbidity increases with hard tumors adherent to critical surrounding structures and these require meticulous dissection techniques for tumor retrieval. The magnetic resonance imaging (MRI) appearance of intracranial meningiomas has been described in many papers.[17],[18],[19],[20] The possible association between the MR appearance of these tumors and the intraoperative observations has been reported.[21],[22],[23],[24],[25],[26] In addition, previous studies to correlate MR images with the histopathology of meningiomas differ in their results.[27],[28],[29],[30],[31],[32],[33],[34] These reports have utilized mainly the T1 and T2 sequences for predicting the operative findings and histopathology. Very few have studied the fluid attenuated inversion recovery (FLAIR) images and the corresponding intraoperative tumor characteristics.[21],[26] Hence the purpose of this prospective study was to associate the convention MR signal intensities (T1, T2, and FLAIR) of intracranial meningiomas with their operative consistency and vascularity, to determine whether the MRI sequences could predict the operative plane during tumor excision, and to relate the MRI with the histopathology of the meningioma.
The study was undertaken in the Department of Neurosurgery at our institute between March 2011 and February 2012 after obtaining clearance from the Institute Ethics Committee. Informed consent was taken from all the patients. A total of 70 consecutive patients with radiological diagnosis of intracranial meningioma who underwent surgical excision and confirmed on histopathology were prospectively studied. The patients underwent MRI using a 1.5 or 3.0 T MRI scanner, in addition to computed tomography (CT) scan. The MR scan included T1 spin echo (SE), T2 SE, and FLAIR precontrast sequences, followed by intravenous (IV) injection of 0.1 mmol/kg body weight of gadopentetate dimeglumine; the contrast-enhanced axial T1-weighted MRI was done using SE sequence. MR image analysis MRI signal intensity The MR appearance of the tumors was graded as marked/mild hypointense, isointense, and marked/mild hyperintense both on T1and T2 images compared with that of the gray matter. It was categorized as hypointense, isointense, and hyperintense on FLAIR images. In cases of tumors with heterogeneous signals, the predominant signal intensity was considered for analysis. The T1-weighted enhancement pattern after contrast administration was classified as homogeneous and inhomogeneous. Operative plane on MRI The imaging characteristics to determine the operative plane based on MRI was adopted from the study by Alvernia and Sindou.[24] The radiological parameters assessed were tumor size, meningioma–brain interface, and peritumoral edema. The tumor size was taken as its largest diameter on T1 MRI. On T2-weighted sequences, the meningioma–brain interface was categorized into marked interspace wherein a definite marked space of more than 1 mm wide was present in over half of the surface between the meningioma and adjacent brain; regular margin imaging in which neither a marked interspace nor an irregular margin was noted; however, a regular demarcation between the meningioma and adjacent brain was present in over half of the surface; and irregular margin imaging in which there was no definite demarcation between the meningioma and adjacent brain in over half of the surface. The extent of peritumoral edema, measured from T2 MR sequences was graded as (a) absent, if there was no evidence of hyperintensity around the tumor; (b) focal edema, if the hyperintensity around the tumor was 3 cm or less in width; and (c) lobar/hemispherical edema, if it was extending greater than 3 cm involving the whole lobe or a hemisphere. Operative findings The required intraoperative details were gathered from the operating surgeons. The consistency of the meningioma was classified as soft for tumors that were evacuated with suction or those that could be aspirated using Cavitron ultrasonic surgical aspirator; hard for tumors removed with sharp dissection; and mixed for tumors having both hard and soft components. The tumor vascularity was categorized as mild, moderate, and high. The operative plane during tumor excision as described by Alvernia and Sindou was utilized in our study.[24] It was extrapial if a clear plane was present between the meningioma and the brain outside the pial layer in over two-thirds of the meningioma–brain interface; mixed if a plane was present in more than one-third and less than two-thirds of the meningioma–brain interface; subpial if the dissection was below the pial layer due to the pial adherence with the tumor on more than two-thirds of the meningioma–brain interface. Histopathology The excised specimen was collected, fixed with formalin, and submitted for routine histopathological examination. After histopathological confirmation, meningiomas were categorized according to the World Health Organization (2007) classification. Other pathological features such as calcification, psammomatous bodies, necrotic changes, cystic degeneration, and cellularity were noted. Special stains such as periodic acid Schiff staining were applied in cases of secretory meningiomas. Immunohistochemistry for epithelial membrane antigen, vimentin, and Ki-67 was performed as required to confirm diagnosis in difficult cases. The Statistical Package for the Social Sciences, version 21 was used to analyze the data. The chi-square test was used to associate MRI signals with intraoperative parameters and a histopathological subtype of meningiomas. Multivariate analysis was performed using logistic regression to find the independent relationship between MR signal intensities and study variables. A P value of < 0.05 was considered significant.
The mean age of our patients was 46 years (range 15–75 years). Among males and females, it was 46.4 (15–70) and 45.8 years (28–75), respectively. Of the overall 70 patients, 26 (37%) were males and 44 (63%) were females with gender ratio of 1:1.7. The distribution of meningiomas was as follows: convexity (26%), parasagittal (19%), falcine (16%), skull base (26%), and posterior fossa (14%). Recurrent meningiomas constituted about 10%, and 3% had multiple meningiomas. Simpson grade I excision was performed in 24% of patients; 49% had Simpson grade II excision; 11% and 16% underwent Simpson grade III and grade IV excision, respectively. There was significant association between tumors located at the skull base and the grade of excision. The various MR signal intensities of meningiomas and their relationship to study variables are shown in [Table 1], [Table 2], [Table 3]. The representative images of the study parameters on MRI are provided in [Figure 1]. On T1-weighted MR images, 10% of meningiomas were markedly hypointense and 29% were mildly hypointense to gray matter. In addition, 57% were isointense and 4% were mildly hyperintense to gray matter. On T2-weighted MR sequences, 3% and 17% showed marked and mild hypointensity, respectively; 27% of tumors were isointense, 43% were mildly hyperintense, and 10% were markedly hyperintense to gray matter. Among the FLAIR sequences, tumors were hypointense in 11%, isointense in 39%, and hyperintense in 50%. In T1-weighted postcontrast sequences, the enhancement was homogeneous in 70% and inhomogeneous in 30% of the tumors.
Of the 70 study cases, the tumor was soft in 33% of patients. A hard consistency was found in 27%, and 40% were of the mixed type. On T1 and T2-weighted imaging, no association was found between the signal intensity and consistency of meningiomas. Analyzing the FLAIR images, a hard consistency was noted in 63% of hypointense tumors. There was significant association between FLAIR imaging and the consistency of meningiomas with hypointense tumors being hard intraoperatively (P < 0.05). The inhomogeneous enhancement pattern of meningiomas was also significantly associated with a hard consistency at surgery (P < 0.05). The tumor was mildly vascular in 21% and moderately vascular in 47% of patients. High vascularity was noted in 31% of cases. The extent of tumor vascularity significantly correlated with FLAIR intensity scores but not with T1 and T2-weighted images (P < 0.05). FLAIR hypointense tumors (63%) showed mild vascularity whereas only 11% of hyperintense tumors were mildly vascular and the rest of hyperintense meningiomas had moderate to high vascularity (54% and 34%, respectively). Overall, about three-fourths (74%) of the cases could be resected by an extrapial plane of dissection. Subpial clearance was performed in 11% of patients. The remaining patients (14%) had mixed plane at surgery. T1 and T2-weighted images did not have any relationship to operative plane during surgery. However, FLAIR imaging correlated with the operative plane of meningiomas (P < 0.05), where 63% of FLAIR hypointense tumors had suboptimal plane (subpial and mixed) as compared with only 22% and 20% in isointense and hyperintense group, respectively. Also, the skull base location of tumors and recurrence had significant association with suboptimal plane at surgery (P < 0.05). The size of tumor determined on T1 MR images was <3 cm in 4% and >6 cm in 24% of patients. In 71%, the size ranged from 3 to 6 cm. The correlation between the tumor size and vascularity was significant (P < 0.05). No significant association was identified between the tumor size and consistency as well as its surgical plane. On T2-weighted images, marked interspace between the meningioma and brain surface could be identified in 40% of patients. Regular margin was noted in 47% and the remaining 13% had an irregular margin with respect to the meningioma–brain interface. Meningiomas with marked and regular interface on T2-weighted MRI could be excised by an extrapial plane in 79 and 82% of cases, respectively. Only 7% and 6% with these clear interfaces had subpial resection, whereas 44% of those with irregular interface were found to require a subpial plane of resection. This relationship between T2-weighted meningioma–brain interface and the intraoperative plane was statistically significant (P < 0.05) [Figure 2].
Based on T2-weighted MRI sequences, peritumoral edema was focal in 47% of cases. Lobar or hemispherical edema was observed in 26% of patients and edema was absent in 27% of cases. No association was found between peritumoral edema and the surgical plane of cleavage as well as other study variables. In this study, the most common histological subtype identified was meningothelial meningioma (59%). The transitional variety accounted for 20% of tumors. Other less common histological subtypes were fibroblastic in 7%, psammomatous in 6%, and secretory in 3% of the cases. Representative histopathological sections are shown in [Figure 3]. Single cases of microcystic, angiomatous, papillary, and atypical meningioma were also present (1% each). T1-weighted imaging showed no correlation with histology of meningiomas, whereas T2 and FLAIR images correlated significantly with histopathological subtype (P < 0.05). Fibroblastic and psammomatous subtypes tend to be hypointense on T2 and FLAIR imaging.
Variables found to be significant on univariate analysis were subjected to logistic regression analysis [Table 4]. On multivariate analysis, FLAIR hypointensity and the skull base location of meningiomas had a significant independent association with suboptimal surgical plane (P < 0.05). The skull base location of tumors had a significant association with the extent of excision (P < 0.05). Among MRI sequences, FLAIR hypointensity had the highest specificity of 94% to predict suboptimal surgical plane.
Preoperative radiological evaluation of meningiomas is useful in anticipating their likely intraoperative nature. Both CT and MRI are useful imaging modalities in such respect. The MRI sequences provide information about the possible consistency, vascularity, and operative plane of tumor.[21],[22],[23],[24],[25],[26] In addition, the pattern of contrast enhancement and enhancing vascular structures could suggest the vascularity and blood supply of the tumor. On the contrary, CT is better than MRI in delineating the extent of bony involvement such as hyperostosis or adjacent calvarial erosion. Bony involvement in meningiomas is commonly hyperostosis, which are seen in about 20%.[35] Occasionally, there can be osteolytic changes and direct invasion of bone. Thus, CT evaluation can complement MR images and both have to be thoroughly studied together before attempting on excision of meningiomas. The focus of this paper was to study the predictive value of conventional MR images (T1, T2, and FLAIR), with respect to the intraoperative features of meningiomas. We intended to study these routine MR sequences so that these could be of value in resource-constrained settings where advanced MR techniques are not available. The usual appearance of meningiomas on T1 MR images is isointense or hypointense relative to gray matter. On T2 MR images, they are isointense to hyperintense and few are hypointense relative to gray matter.[17] Various reports have attempted to identify the MR signal characteristics that could predict the operative findings and histopathology of meningiomas.[21],[22],[23],[24],[25],[26],[27],[28],[29],[30],[31],[32],[33],[34] The consistency of the meningioma becomes relevant in view of the greater operative time reported in hard tumors, especially when tumors are large or adherent to critical neurovascular structures.[22] Our study showed no correlation of T1 and T2-weighted MR signals with the consistency of meningiomas. However, significance was observed with FLAIR images; tumors which were hypointense tended to be hard in about two-thirds of the cases. The literature shows reports relating to MR signal intensities with the consistency of meningiomas. Although the T1 MR images were nonspecific, the signal intensity on T2 or a combination of MR sequences was found to correlate with consistency of the meningiomas.[21],[22],[23],[29],[30] Tumors with hypointensity on T2 and FLAIR images were hard and fibrous, and those with a high signal intensity were soft in consistency.[21],[22] In addition, hyperintensity on proton density sequence as also predictive of a soft tumor.[23] Chen et al. and Zee et al. studied that T2 hyperintensity was related to soft, hypervascular and aggressive, angioblastic meningiomas.[29],[30] The T2 hyperintense appearance is attributed to the high water content and cellularity of the soft tumors.[22],[23],[27] On the contrary, an Italian study reported no correlation of MR signal intensity with the consistency of meningiomas.[32] Studies have shown that hyperintense tumors on T2 MR images were associated with high vascularity.[27],[29] In our patients, though there was no association with T2 imaging, FLAIR hypointense tumors showed less vascularity. Some authors have tried to predict the operative plane of meningiomas using preoperative imagings such as MRI and angiography.[24],[25],[26] The plane of dissection in a meningioma surgery is dependent on the tumor size, peritumoral edema, and pial-cortical vascularization. This in turn predicts the clinical outcome.[3],[14],[24],[25],[26] A Turkish study could predict the plane during meningioma surgery based on T2 MRI.[25] In the present study, we found that on multivariate analysis FLAIR hypointensity of tumors could be an independent predictor of suboptimal intraoperative plane. For the ease of comparison, the T2-based meningioma–brain interface in our study, which was determined using the same criteria as by Alvernia and Sindou, correlated with the operative plane of tumors. Over three-fourths of the tumors with a marked and regular T2 interface had an extrapial surgical plane. However, Alvernia and Sindou in their report failed to prove any association between the tumor cortex interface and the operative plane at surgery.[24] A study which evaluated the tumor–cortex interface by T1, T2 as well as FLAIR imaging reported that the preoperative identification of a rim at the interface predicted a lesser degree of tumor adhesion to the brain at surgery.[26] This study did not find any association between the size of the tumor and the operative plane in contrast to that reported by Alvernia and Sindou.[24] However, the tumor size was found to correlate with its vascularity. Studies have reported a correlation of peritumoral edema with surgical plane of cleavage.[24],[25],[26] In the report by Ildan et al., the severity of the peritumoral edema correlated with the pial-cortical blood supply to the meningioma.[25] The greater the extent of the edema surrounding the tumor, the higher the possibility of cortical penetration and a subpial resection.[24],[25],[26] However, the present study did not show any significant relationship between the two. Though not studied by us, evidence from other reports suggests that the pial-cortical predominant vascularization of meningiomas correlates with subpial plane at surgery.[24],[25],[26] In the present study, T2 and FLAIR hypointense imaging was associated with fibroblastic and psammomatous subtypes of meningiomas. Previous results vary with respect to correlation between MR signal intensity and histopathology of meningiomas.[27],[28],[29],[30],[31],[32],[33],[34] A T2-based MR correlation has been reported by Elster et al. and Maiuri et al.[27],[28] In their series, T2 hypointense tumors had more of fibroblastic and transitional subtypes; T2 isointense tumors generally comprised transitional with some amount of fibroblastic and syncytial variety; T2 hyperintense tumors were syncytial and angioblastic, with high vascularity and a soft consistency. Suzuki et al. showed that fibroblastic tumors were hypointense and hard while angioblastic meningiomas were soft and had higher signal intensity on T2-weighted images. With regard to meningothelial meningioma, the most common histopathological subtype, a clear correlation was not arrived at in the same study.[22] A Belgian study concluded that though the histological subtypes have different MRI features, it was insufficient to predict histological diagnosis by MRI alone.[31] Similarly, there are other reports that could not find any relationship between MR signals and histology of meningiomas.[23],[33],[34] An Italian study also reported no significant correlation of MR signal intensity with histology. However, they had noted that no fibroblastic meningioma was hyperintense on T2-weighted sequence.[32] Contrast enhancement did not bear any relationship to the histopathological subtype in our study similar to other reports.[27],[29] A preoperative assessment of the described radiological features of a meningioma using the conventional MRI sequences may help the surgeon in planning the surgery, and to anticipate its difficulty even in with a lack of advanced neuroimaging techniques. In patients with good brain-tumor interface and other favorable factors in MRI, limited bony exposure with minimal access techniques may be considered, as the likelihood of postoperative edema is decreased.[36] On the contrary, if there is poor tumor interface in preoperative MRI, patients may need a larger craniotomy to take care of postoperative edema.
FLAIR hypointense appearance of meningiomas turned out to be an independent factor associated with the suboptimal plane during surgery. It had a high specificity and could predict the operative plane of meningiomas. The skull base location of tumors influence the operative plane and the extent of excision. Financial support and sponsorship Nil. Conflicts of interest There are no conflicts of interest.
[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3], [Table 4]
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