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Journal of Korean Neurosurgical Society > Volume 63(5); 2020 > Article
Kim, Kim, Ji, Kang, Kim, Kim, Park, Choi, and Park: Intracranial Metaplastic Meningioma : Clinical and Radiological Characteristics of 11 Cases

Abstract

Objective

Metaplastic meningioma is an extremely rare subtype of World Health Organization (WHO) grade I meningioma. It has distinctive histological subtypes according to its own mesenchymal components. Owing to its scarcity, clinical or radiological features of a metaplastic meningioma are poorly described.

Methods

Between 2004 and 2018, we analyzed total 1814 cases surgically proven meningioma for 15 years. Among them, metaplastic meningioma was diagnosed in 11 cases. Magnetic resonance images were taken for all patients, and computed tomography scan was taken for 10 patients.

Results

WHO grade I meningiomas were 1376 cases (75.9%), 354 cases (19.5%) in WHO grade II, and 84 cases (4.6%) in WHO grade III meningiomas. Metaplastic meningioma was 11 cases as 0.8% of WHO grade I meningioma and 0.6% of entire meningiomas for 15 years. Among the entire 11 metaplastic meningiomas, five tumors (45%) were diagnosed as a lipomatous subtype with rich fat components, four (36%) as an osseous subtype with extensive bone formation and two (18%) as a xanthomatous subtype. There was no cartilaginous subtype metaplastic meningioma in our study. Lipomatous and osseous metaplastic meningioma have peculiar radiological characteristics according to mesenchymal components.

Conclusion

We investigated a rare metaplastic meningioma subtype based on our 15-year surgical experience with meningiomas. Further investigation will be necessary for the clear clarification of tumor nature of this rare tumor.

INTRODUCTION

World Health Organization (WHO) grade I benign meningioma includes nine subtypes : meningothelial, fibrous, transitional, psammomatous, angiomatous, microcystic, secretory, lymphoplasmacyte-rich, and metaplastic meningioma [1,5,6,8,9,19,21]. Among these, metaplastic meningioma is an extremely rare subtype, defined as containing focal or widespread mesenchymal components including osseous, cartilaginous, lipomatous, and myxoid or xanthomatous tissue, singly or in combination [1,2]. In addition, metaplastic meningiomas are often referred to as lipomatous, osseous or xanthomatous, based on their dominant mesenchymal components [19].
The clinical and radiological characteristics of meningiomas, the most common extraaxial primary brain tumor, have been widely described. The unique radiological features associated with their histology have also been delineated. Microcystic meningioma, characterized by the formation of intercellular microcysts, show the distinguishing radiological feature of markedly high signal intensity with severe peritumoral edema in T2-weighted images [4,13,16]. Sclerosing meningioma also show peculiar radiological features, such as very low signal intensity on T2-weighted images due to their abundant calcification [10]. Secretory meningioma are characterized by an intracellular lumen containing an eosinophilic secretion (i.e., a pseudopsammoma body), which shows a characteristic high intensity in up to 96% of cases. They may also exhibit relatively high apparent diffusion coefficient values compared with typical meningiomas [11,13].
Due to their rarity, the clinical and radiological features of metaplastic meningiomas have been poorly described. Thus, the study goal was to systematically review all available surgically confirmed metaplastic meningiomas at our center, to determine whether they have unique clinical and/or radiological characteristics.

MATERIALS AND METHODS

This study was performed in accordance with the ethical standards of the International Research Board of Seoul National University (IRB No. H-2005-163-1125). We retrospectively analyzed patients whose diagnosis with meningioma was surgically confirmed at our institute between 2004 and 2018, during which time 1814 total cases were identified. Eleven consecutive cases were found to have been pathologically confirmed as metaplastic meningioma. These patients’ clinical, radiological, histopathological, and surgical records were obtained from electronic databases and reviewed in detail. These patients (four males and seven females) had a mean age of 60 years.
For radiological analyses, preoperative magnetic resonance (MR) and computed tomography (CT) images were collected, including: attenuation (high, iso-dense, low), calcification, and fat component (absent versus present) for CT images; T1- and T2-weighted signal intensity (high, iso, or low), enhancement pattern (homogeneous versus heterogeneous), and peritumoral edema (absent versus present) were collected for MR images. Histopathological reviews were repeated by a neuropathologist.

RESULTS

From 2004 to 2018, a total of 1814 surgically confirmed meningioma cases were seen at our institute. Metaplastic meningioma was diagnosed in 11 cases, representing 0.8% of WHO grade I meningioma and 0.6% of all meningiomas during the 15-year study period. The details of these meningioma grades and subtypes are shown in Fig. 1.

Illustrative case 1

A 54-year-old woman visited the outpatient clinic for evaluation of a brain tumor that had been incidentally detected following a traffic accident. She had no neurological symptoms or signs. Brain CT showed a 4.8 cm heterogeneously isodense lesion surrounded by a hypodense edge on the left frontal convexity and a 3.4 cm bony mass with ground-glass opacity on the left frontal bone. MR images revealed a 4.8 cm mass with heterogeneous isosignal intensity in T2-weighted images suggesting the involvement of fatty components. The mass appeared as a heterogeneously enhancing lesion after contrast administration. Despite the tumor size, definite peritumoral edema was absent. The primary preoperative radiological diagnosis was meningioma with teratoma or fatty components, though teratoma could not be excluded (Fig. 2A-D).
After a typical frontal craniotomy, a grey-whitish hard mass was visualized and internal debulking was accomplished with a Cavitron ultrasonic surgical aspirator. The tumor was completely removed after extracapsular dissection superiorly, anteriorly, and medially. The patient was discharged without neurological deterioration.
Upon microscopic examination, the mass was a poorly circumscribed lesion with multinodular lobular architecture. The tumor cells had abundant eosinophilic cytoplasm and uniform, round-to-oval nuclei with minimal cytology atypia. Whorl formation was frequently observed. Adipocytic proliferation was noted within the lobules and in the surrounding stroma. Immunohistochemistry of the tumor cells showed strong membrane positivity to epithelial membrane antigen.
Other microscopic features showed only increased cellularity. There was no brain invasion, foci of spontaneous necrosis, uninterrupted patternless or sheet-like growth, prominent nucleoli, or small cells with a high nucleus/cytoplasm ratio. The mitotic count was 3 per 10 high power fields. The final pathologic diagnosis was metaplastic meningioma with rich fat component. The detailed pathological features are shown in Fig. 3.

Illustrative case 2

A 37-year-old woman suffering from a headache over several weeks presented generalized tonic-clonic seizure. Brain CT showed a 4.2 cm heterogeneously hyperdense lesion on the right frontal lobe suggesting calcification. Brain MR images also revealed heterogeneously high intensity on T1-gadolinium enhanced images (Fig. 2E-H). Preoperative radiological diagnosis was meningioma with dense calcification.
Frontal craniotomy was performed as usual, yellowish firm mass with dense calcification was revealed. The total removal of mass was accomplished, and the patient was discharged after seizure-free status. Histopathological examination showed that the tumor had diffuse osseous metaplasia with brain invasion. The tumor was finally diagnosed WHO grade I a metaplastic meningioma with osseous metaplasia.

Summary of metaplastic meningioma cases

The clinical, radiological, and histopathological details of all 11 patients are summarized in Table 1. There were four male and seven female patients, with a mean long tumor diameter of 4.8 cm (range, 3.4-6.2) and mean age of 60 years (range, 24-65).
Detailed subclassification of the 11 metaplastic meningiomas showed that five cases were lipomatous, four osseous, and two xanthomatous subtypes. In our 15-year meningioma survey, lipomatous meningioma was the most common subclass of metaplastic meningioma. Cartilaginous subtype was also found in our patient population.
We found no common or unique radiological characteristics among all metaplastic meningiomas. However, obvious calcification on CT and marked fat signal intensity on MR images were detected in the osseous-type and lipomatoustype metaplastic meningiomas, respectively.

DISCUSSION

Although meningioma are the most common primary extra-axial tumors, some subtypes are unfamiliar to many neurosurgeons. This is primarily due to their low incidence, especially since WHO grade I meningioma include nine subtypes, based on their histopathological features. Among these, metaplastic meningioma is among the rarest. In 2018, Zouaoui and colleagues [22] reported a nationwide descriptive epidemiology of meningioma. In their 15-year study in France, the incidence of metaplastic meningioma was 0.04% (62 of 13038 newly diagnosed and histologically confirmed meningioma). Another epidemiologic study also showed the extreme rarity of metaplastic meningioma, with an incidence of 0.21% (15 of 7084 cases) [18]. Similarly, the proportion of metaplastic meningioma was 0.8% in our 15-year surgical experience with meningiomas. Thus, our data reconfirm that it is among the rarest meningioma subtypes.
Another notable study finding was our initial evaluation of meningioma distribution according to WHO grade. During our 15-year study period, WHO grade I meningioma accounted for 1376 (75.9%) cases : 354 (19.5%) and 84 (4.6%) cases were WHO grades II and III, respectively. The two epidemiologic studies described above reported 89.2% and 91.9% WHO grade I, 9.3% and 5.2% WHO grade II, and 1.5% and 2.9% WHO grade III meningioma, respectively [20,22]. Thus, our incidence rates of WHO grades II and III meningiomas appear slightly higher than those reported previously. However, we must acknowledge several inherent study limitations. The study was retrospective and conducted at a single-center over 15 years. Possible selection bias was included due to the rarity and heterogeneity of metaplastic meningioma and the protocol did not reflect changes over time in the WHO classification criteria.
Metaplastic meningioma is referred to by several different names based on the presence of metaplastic changes to the dominant mesenchymal component : osseous, lipomatous, cartilaginous, myxoid and xanthomatous meninigoma [21]. The term ‘metaplastic’ is used because the transformed neoplastic cells demonstrate the full histological characteristics of the cells they mimic [19]. Lipomatous metaplastic meningioma are made up of adipocyte resembling fatty cells with a signet-ring appearance [3,6,21]. Myxoid metaplastic meningioma are characterized by their excessive hyaluronic acid and chondroitin sulfate [5,7,9,12]. Osseous subtypes are confirmed by the presence of mature bone tissue and tumor cells in regions containing no psammoma bodies [1,14,15,17,18]. A recent literature review by Choi et al. [2] described 26 metaplastic meningiomas, including 12 osseous subtypes, nine lipomatous subtypes, four xanthomatous subtypes, and one cartilaginous subtype. In our study, we were able to identify subtypes within the 11 metaplastic meningiomas, including nine lipomatous, four osseous, and two xanthomatous. No cartilaginous metaplastic meningioma was identified. Most metaplastic meningioma in our study were lipomatous or osseous metaplastic meningioma, similar to previous studies.
On radiological examination, the lipomatous type metaplastic meningioma demonstrated peculiar radiological features associated with a fatty component (Table 1, case 1 of Fig. 2). Although calcification is commonly observed in a meningioma, osseous type metaplastic meningioma had a distinct calcification on CT and MR images (Table 1, case 9 of Fig. 2). No other unique clinical characteristics of metaplastic meningioma were found.
The primary study purpose was to determine whether metaplastic meningiomas have unique clinical or radiological characteristics. We were unable to identify any unusual characteristics that might help distinguish metaplastic meningioma from other meningioma subtypes. However, toward further defining metaplastic meningioma, we note some common radiological and histological characteristics, such as the representative cases of lipomatous and osseous metaplastic meningioma. Despite the study limitations described above, we expect this study to confer a better understanding of the nature of these rare tumors.

CONCLUSION

We investigated a rare metaplastic meningioma subtype based on our 15-year surgical experience with meningiomas. Metaplastic meningiomas are classified based on their mesenchymal components, some of which have unique radiological characteristics. Further investigation will be necessary to describe the nature of these rare tumors more clearly.

Notes

No potential conflict of interest relevant to this article was reported.

INFORMED CONSENT

This type of study does not require informed consent.

AUTHOR CONTRIBUTIONS

Conceptualization : TK, JWK

Data curation : TK, SYJ, HK, KMK, SHC, SHP

Formal analysis : TK, JWK, SHP

Methodology : YHK, CKP, JWK

Project administration : JWK

Visualization : TK

Writing - original draft : TK, JWK

Writing - review & editing : YHK, CKP, JWK

Fig. 1.
Distribution of surgically proven meningioma cases from 2004 to 2018 according to WHO grade. There were 1376 (75.9%) WHO grade I benign meningioma cases; 354 (19.5%) and 84 cases (4.6%) were WHO grades II and III, respectively. Among the WHO grade I meningioma, meningothelial subtype was the most common, occurring in 644 of 1376 cases (46.8%). The second most common subtype was transitional meningioma (372 cases, 27.0%), followed by fibrous, microcystic, and psammomatous subtypes. Relatively rare with less than 2% incidence were sclerosing, secretory, metaplastic and lymphocyte-rich meningiomas. Metaplastic meningioma was diagnosed in 11 cases, representing 0.8% of WHO grade I meningioma and 0.6% of all meningiomas during the 15-year study period. The rarest was lymphocyte-rich subtype, with only three cases (0.2%). WHO : World Health Organization.
jkns-2020-0151f1.jpg
Fig. 2.
A-D : Preoperative CT and MR images of lipomatous meningioma (case 1). White arrow suggesting the involvement of fatty components. E-H : Osseous meningioma (case 9). CT : computed tomography, MR : magnetic resonance.
jkns-2020-0151f2.jpg
Fig. 3.
Gross photo of the surgically resected specimen (formalin-fixed overnight). B : Representative microscopic image shows admixed meningioma tumor cells and fat component (hematoxylin & eosin stain, ×40). C : Membrane immunoreactivity of epithelial membrane antigen immunohistochemical stain observed (×100). D : Ki-67 immunohistochemical stain reveals low proliferative index of tumor cells (Positive in 5%, ×100).
jkns-2020-0151f3.jpg
Table 1.
Summary of clinical, histopathological and radiological data of consecutive 11 patients with a metaplastic meningioma
No Gender/age Initial symptom Location Long diameter (mm) Extent of resection Last follow-up (months) CT
MRI
Mitotic count (per 10 high power filed) Ki-67 (%) WHO grade Detailed subtype
Calcification T2 Fat component
1 F/54 Incidentally found Left frontal convexity 50 GTR 31 No High Yes 3 5.62 I Lipomatous
2 M/37 Seizure Left parietal convexity 53 NTR 12 No High Yes <1 1 I Lipomatous
3 M/48 Incidentally found Left parietal convexity 40 GTR 72 No High Yes 1 5.67 I Lipomatous
4 F/69 Weakness Midline falx 53 GTR 17 No High Yes <1 6.8 I Lipomatous
5 M/65 Motor dysphasia Left frontal convexity 49 GTR 34 Yes High Yes 1 2.12 I Lipomatous
6 F/60 Visual symptom Anterior falx 62 GTR 136 Yes High No NA NA I Osseous
7 M/62 Headache Midline subfrontal area 34 GTR 36 Yes Low No <1 1 I Osseous
8 F/37 Seizure Right frontal convexity 44 NTR 68 Yes High No 1 0.3 I Osseous
9 F/55 Headache Midline falx 37 NTR 34 Yes Low No <1 0.63 I Osseous
10 F/27 Headache Anterior parasagittal 54 NTR 150 No High No 3 4.6 I Xanthomatous
11 F/61 Incidentally found Parasagital 44 GTR 34 NA High No 1 5 I Xanthomatous

CT : computed tomography, MRI : magnetic resonance image, WHO : World Health Organization, F : female, GTR : gross total resection, M : male, NTR : near total resection, NA : not available

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