DNA methylation profiling of a lipomatous meningioma: illustrative case

Zeel Patel Temerty Faculty of Medicine, University of Toronto, Toronto, Ontario, Canada

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Justin Z. Wang MacFeeters Hamilton Neuro-Oncology Program, Princess Margaret Cancer Centre, University Health Network and University of Toronto, Toronto, Ontario, Canada
Division of Neurosurgery, Department of Surgery, University of Toronto, Toronto, Ontario, Canada; and

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Zamir Merali MacFeeters Hamilton Neuro-Oncology Program, Princess Margaret Cancer Centre, University Health Network and University of Toronto, Toronto, Ontario, Canada
Division of Neurosurgery, Department of Surgery, University of Toronto, Toronto, Ontario, Canada; and

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Vikas Patil MacFeeters Hamilton Neuro-Oncology Program, Princess Margaret Cancer Centre, University Health Network and University of Toronto, Toronto, Ontario, Canada

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Farshad Nassiri MacFeeters Hamilton Neuro-Oncology Program, Princess Margaret Cancer Centre, University Health Network and University of Toronto, Toronto, Ontario, Canada
Division of Neurosurgery, Department of Surgery, University of Toronto, Toronto, Ontario, Canada; and

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Qingxia Wei MacFeeters Hamilton Neuro-Oncology Program, Princess Margaret Cancer Centre, University Health Network and University of Toronto, Toronto, Ontario, Canada

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Julio Sosa MacFeeters Hamilton Neuro-Oncology Program, Princess Margaret Cancer Centre, University Health Network and University of Toronto, Toronto, Ontario, Canada

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Claire Coire Division of Neuropathology, Department of Pathology, Trillium Health Partners, Mississauga, Ontario, Canada

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Gelareh Zadeh MacFeeters Hamilton Neuro-Oncology Program, Princess Margaret Cancer Centre, University Health Network and University of Toronto, Toronto, Ontario, Canada
Division of Neurosurgery, Department of Surgery, University of Toronto, Toronto, Ontario, Canada; and

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BACKGROUND

Lipomatous meningiomas are an extremely rare, benign meningioma subtype subcategorized under metaplastic meningioma in the most recent 2021 update to the World Health Organization classification. They make up less than 0.3% of all meningiomas and, to date, less than 70 cases have been reported in the literature, none of which have undergone molecular profiling. This study aims to promote the utility of molecular profiling to better diagnose these rare tumors.

OBSERVATIONS

The authors present the first case of a lipomatous meningioma with DNA methylation profiling that both confirmed its benign biology and uncovered unique cytogenetic changes. Molecular characterization of a lipomatous meningioma confirmed its diagnosis as a distinct, benign meningioma subtype and revealed several copy number variations on chromosome 8 and in NF2 and SMARCB1. Here we discuss some of the radiological and histopathological features of lipomatous meningiomas, how they can be used to distinguish from other meningiomas and other similarly presenting tumors, and a brief literature review discussing the pathophysiology and presentation of this rare tumor.

LESSONS

This study provides evidence supporting the use of molecular profiling to diagnose lipomatous meningiomas and guide their clinical management more accurately.

ABBREVIATIONS

CNS = central nervous system; CNV = copy number variation; CT = computed tomography; DKFZ = Deutsches Krebsforschungszentrum; EMA = epithelial membrane antigen; IHC = immunohistochemical; MRI = magnetic resonance imaging; STAT6 = signal transducer and activator of transcription 6, interleukin-4 induced; T1W = T1-weighted; T2W = T2-weighted; WHO = World Health Organization

BACKGROUND

Lipomatous meningiomas are an extremely rare, benign meningioma subtype subcategorized under metaplastic meningioma in the most recent 2021 update to the World Health Organization classification. They make up less than 0.3% of all meningiomas and, to date, less than 70 cases have been reported in the literature, none of which have undergone molecular profiling. This study aims to promote the utility of molecular profiling to better diagnose these rare tumors.

OBSERVATIONS

The authors present the first case of a lipomatous meningioma with DNA methylation profiling that both confirmed its benign biology and uncovered unique cytogenetic changes. Molecular characterization of a lipomatous meningioma confirmed its diagnosis as a distinct, benign meningioma subtype and revealed several copy number variations on chromosome 8 and in NF2 and SMARCB1. Here we discuss some of the radiological and histopathological features of lipomatous meningiomas, how they can be used to distinguish from other meningiomas and other similarly presenting tumors, and a brief literature review discussing the pathophysiology and presentation of this rare tumor.

LESSONS

This study provides evidence supporting the use of molecular profiling to diagnose lipomatous meningiomas and guide their clinical management more accurately.

ABBREVIATIONS

CNS = central nervous system; CNV = copy number variation; CT = computed tomography; DKFZ = Deutsches Krebsforschungszentrum; EMA = epithelial membrane antigen; IHC = immunohistochemical; MRI = magnetic resonance imaging; STAT6 = signal transducer and activator of transcription 6, interleukin-4 induced; T1W = T1-weighted; T2W = T2-weighted; WHO = World Health Organization

Meningiomas are the most common primary intracranial tumor, comprising approximately one-third of all brain tumors. Symptoms can vary depending on the size and anatomical location of the tumor but can include headaches, seizures, neurological deficits, and behavioral changes.1 These tumors are identified usually through magnetic resonance imaging (MRI) or computed tomography (CT), often following the development of neurological symptoms or incidentally in asymptomatic patients on imaging obtained for other clinical purposes.2

While molecular profiling has complemented histopathology in the diagnosis of other central nervous system (CNS) tumors such as gliomas, the most recent 2021 World Health Organization (WHO) classification still defines meningioma grades (grades 1–3) largely based on histopathological features alone, except for WHO grade 3 meningiomas, which now include supplementary molecular criteria (TERT promoter mutation or homozygous loss of CDKN2A/B).3 Within the WHO grade 1 classification, metaplastic meningiomas remain a rare but important histological subtype of meningioma containing focal or widespread mesenchymal components, including osseous, cartilaginous, myxoid, xanthomatous, or lipomatous tissue alone or in combination with each other. Lipomatous meningiomas are the rarest subtype of metaplastic meningioma, with only 67 cases reported in the literature so far, most of which have limited clinical follow-up, and none of which have had molecular profiling performed.4 In lipomatous meningiomas, meningothelial cells on histopathology usually resemble typical meningiomas interspersed with lipomatous regions where cells resemble adipocytes or lipoblasts. These lipomatous cells and can be discerned from adipose tissue by the immunohistochemical (IHC) expression of epithelial membrane antigen (EMA), somatostatin receptor 2A (SST2A), vimentin, and progesterone, and the absence of glial fibrillary acidic protein (GFAP), an astrocyte marker.5–7 However, histopathology and IHC may be prone to interrater variability at times.8 Since numerous recent studies have shown that molecular alterations in meningiomas, including DNA methylation and copy number alterations, can predict meningioma biology and clinical behavior more accurately than WHO grade alone,9–11 this variability may be ameliorated by incorporating molecular profiling in addition to histopathology. Here we report on the first DNA methylation analysis on a lipomatous meningioma in the literature to demonstrate that DNA methylation profiles can be used to reliably classify this distinct subtype of meningioma, predict its benign course, and identify unique cytogenetic changes that differentiate it from other more commonly seen meningiomas clinically. We correlate these findings to histopathological and IHC findings from our own case as well as cases in the literature to provide a comprehensive review on the diagnosis and management of patients with lipomatous meningiomas.

Illustrative Case

A 71-year-old female presented with a primary complaint of headaches for several months. She had a history of migraines, but the headaches began escalating in severity and frequency, were exacerbated by Valsalva maneuvers, and were associated with nausea and light-headedness but no focal neurological deficits or auras. All other history was noncontributory.

Investigations

Urgent MRI was performed with limited sequences and without gadolinium, which showed a right cerebellar convexity extra-axial lesion that was heterogeneous and hyperintense on T1-weighted (T1W) sequences and hypodense on T2-weighted (T2W) sequences, measuring approximately 4 cm in maximal diameter and causing mass effect on the adjacent cerebellum with some perilesional edema (Fig. 1A and B). These imaging findings were suggestive of a cerebellar convexity meningioma. Given the large size of the tumor and progressive symptomatology suggestive of elevated intracranial pressure, resection was recommended. A posterior fossa craniotomy was performed, and gross-total resection of the tumor and its dura attachments was performed without any complications (Fig. 1C). During surgery, the mass was noted to be unusually soft and yellow in appearance.

FIG. 1.
FIG. 1.

A: Preoperative axial cranial T1W MRI without gadolinium showing a hyperintense, heterogeneous, extra-axial lesion in the right cerebellar convexity. B: Preoperative sagittal cranial T2W MRI demonstrating a cerebrospinal fluid cleft and some adjacent perilesional edema. C: Postoperative axial cranial CT demonstrating complete macroscopic resection of this mass.

Histopathology

On histopathological analysis, the tumor displayed some areas typical of a meningioma but also extensive lipomatous metaplasia (Fig. 2A). On immunostaining, the tumor cells were EMA positive (Fig. 2B) and signal transducer and activator of transcription 6, interleukin-4 induced (STAT6) negative (Fig. 2C). There were no atypical features, including no mitoses, no brain invasion, no increased cellularity, no sheeting, no small cell formation, and no prominent nucleoli. Together, these findings seemed to corroborate a diagnosis of a lipomatous meningioma.

FIG. 2.
FIG. 2.

Histopathological microscopic imaging of the lipomatous meningioma case. Each image is 8× the original magnification with a 20× image embedded within. A: H&E staining illustrates meningothelial cell morphology and mature adipocyte-like cells with flattened, peripherally placed nuclei. B: EMA cytoplasmic immunostaining is positive. C: STAT6 nuclear immunostaining is negative.

DNA Methylation

DNA was extracted from formalin-fixed paraffin-embedded tumor tissue using the DNeasy Blood and Tissue Kit (Qiagen) and quantified using the Nanodrop 1000 Instrument (Thermo Fisher Scientific). Methylation profiling was performed using the Illumina Infinium Methylation EPIC BeadChip Array (Illumina) on 500 ng of bisulfite-converted DNA (EZ DNA methylation kit, Zymo), as previously published.9,10 Raw methylation file (.idat) processing and quality control were performed as previously described and methylation files were uploaded to the open-access Deutsches Krebsforschungszentrum (DKFZ) DNA methylation brain tumor classifier12 and to the Toronto Meningioma Recurrence Score site.13 The DKFZ classifier version 12.5 classified the tumor as a meningioma with a calibrated score of 0.99504 (Fig. 3A), specifically belonging to a benign methylation class with a calibrated score of 0.99404. However, calibrated scores did not meet the cutoff for any specific methylation-based benign subclass. Copy number analysis and plot demonstrated a relatively low number of cytogenetic changes but did include losses in chromosome 8 and chromosome 22q (including loci for NF2 and SMARCB1), as well as partial gains of chromosomes 5, 7, 13q, and 14q (Fig. 3B).14 A t-distributed stochastic neighbor embedding plot (t-SNE) demonstrated clustering of this lipomatous meningioma with other meningioma reference cases from the DKFZ classifier version 11.4 on the basis of its DNA methylation profile (Fig. 3C). When analyzed using the Toronto Meningioma Recurrence score and previously published recurrence risk nomogram, this meningioma was noted to have a very low risk of recurrence at < 1% within 5 years based on its methylome alone and < 10% based on the combination of WHO grade, Simpson grade, and its tumor methylome (Fig. 3D and E).13 Altogether, these findings suggest that, using DNA methylation, lipomatous meningioma can (1) be reliably classified as a meningioma due to a common cell of origin with other meningiomas, (2) be predicted to have a benign progression, in keeping with the literature, and (3) have unique cytogenetic changes such as loss of chromosome 8 and gain of chromosomes 7 and 14q that have been uncommonly seen in meningiomas previously.

FIG. 3.
FIG. 3.

DNA methylation profiling of lipomatous meningioma. A: DKFZ classifier v12.5 diagnosis class and meningioma subclasses with their respective calibrated score. A calibrated score > 0.8 is required to classify this as a “match.” B: Copy number plot demonstrating gains and losses of chromosome arms from 1 to 22 as well as specific annotated gene loci on these arms. Gains/amplification (green) represent positive deviation and losses (red) represent negative deviation from baseline. Twenty-nine brain tumor relevant gene regions are highlighted. C: A t-distributed stochastic neighbor embedding plot (t-SNE) plot depicting clustering of lipomatous meningioma (red asterisk) most closely with meningioma reference cases (blue) from the DKFZ classifier v11.4. D: Quality-control profile from DNA methylation analysis performed prior to DNA methylation profiling for recurrence risk demonstrating distribution of genome-wide methylation values (Beta) for this sample. E: Tumor recurrence risk using DNA methylation–based recurrence prediction from tumor methylome alone (agnostic to WHO grade and other clinical features) (above) and based on the clinical nomogram published by Nassiri et al.13 A IDH = IDH glioma, subclass astrocytoma; ANA PA = anaplastic pilocytic astrocytoma; ATRT = atypical teratoid/rhabdoid tumor; CHGL = chordoid glioma of the third ventricle; CHORDM = chordoma; CN = central neurocytoma; CNS NB = central nervous system neuroblastoma; CONTR = control tissue; CPH = craniopharyngioma; DLGNT = diffuse leptomeningeal glioneuronal tumor; DMG = diffuse midline glioma; HGNET = high grade neuroepithelial tumor; HMB = hemangioblastoma; IHG = infantile hemispheric glioma; LGG = low grade glioma; LIPN = liponeurocytoma; LYMPHO = lymphoma; MB = medulloblastoma; MC = methylation class; MELAN = melanoma; MELCYT = melanocytoma; MNG = meningioma; O IDH = IDH glioma; subclass 1p/19q co-deleted oligodendroglioma; PGG = paraganglioma; PIN T = pineoblastoma; PITAD = pituitary adenoma; PITUI = pituicytoma; PLASMA = plasmacytoma; PLEX = plexus tumor; PTPR = papillary tumor of the pineal region; PXA = pleomorphic xanthoastrocytoma; RETB = retinoblastoma; SCHW = schwannoma; SFT HMPC = solitary fibrous tumor/hemangiopericytoma; SUBEPN = supendymoma.

Discussion

Literature Review

Sixty-seven cases of lipomatous meningioma were reviewed in the literature (Table 1). The age of these patients ranged from 14 to 90 years and 5 total cases had recurrences after resection. Follow-up data were available for only 35 of these cases, with follow-up times ranging from 1 to 120 months; however even when follow-up data were available, they were often limited and did not provide detailed information on progression-free survival in recurrent cases.4,5,12,15–35 Furthermore, some studies included in the literature are ambiguous as to whether the cases included are true lipomatous meningioma cases or other metaplastic meningioma subtypes. For example, some studies included all 15 cases reported by Tang et al.16 as lipomatous meningioma cases, but Tang et al. describe these cases as metaplastic meningioma, with only 2 of them being lipomatous and with the others being classified as either smooth muscle, osseous, or xanthomatous.16,24 The significance of distinguishing xanthomatous and lipomatous meningioma is unclear as cases have been reported with a combination of features typical for both of types of tissues, suggesting that a transition between the 2 cell types may also occur.15,36 There is also conflicting interpretation of the expression of S-100, a marker for mature adipocytes, with some suggesting that its absence confirms the metaplastic nature of the tumor cells as opposed to them being true adipocytes,5 whereas others reason that the presence of S-100 illustrates the meningothelial differentiation of these cells.20 Molecular characterization may provide clarification of whether lipomatous or lipoblastic meningioma cells have undergone true metaplasia, as has been classically considered,29 or been “lipidized” through molecular aberrations resulting in lipid accumulation, as recent studies suggest,22 and may better elucidate the pathophysiology and aid with classification of these tumors.

TABLE 1.

Summary of clinical features and pathology of lipomatous meningioma reported in the literature

Authors & YearNo. of Cases*Age in Yrs (range)/Sex: No. or Age (yrs)/SexRecurrence/FUImmunostaining (+)Proliferation Index
Roncaroli et al., 20011518 (lipomatous): 10 (meningothelial), 2 (meningothelial atypical), 3 (transitional), 2 (chordoid), 1 (microcystic)Median 60 (14–79)/F: 13, M: 53 (17%); recurrence time: 7, 8, & 24 mos/FU: 1–120 mos (median 22 mos)EMA: (+) in all; S-100: (+)M1B1: < 5% (n = 16), 10% (n = 1), 20% (n = 1)
Tang et al., 20131615 (metaplastic): 2 (lipomatous), 2 (smooth muscle), 9 (osseous), 2 (xanthomatous)Mean 50.67 (22–74)/F: 5, M: 102 (13%), recurrence time: 6 & 12 mos/FU: NAEMA: (+) n = 15, S-100: (±) n = 2, vimentin: (+) n = 15, SMA: (+) n = 2M1B1: ≤ 1% (n = 14), 3% (n = 1)
Yamada et al., 1999171 (secretory w/ lipomatous component)43/FNAEMA: (+)NA
Withers et al., 2003181 (lipomeningoma)61/MNANANA
Mariniello et al., 2000191 (lipomatous)77/FNR/FU: 4 yrsEMA: (+), S-100: (+), vimentin (+)NA
Colnat-Coulbois et al., 2008202 (lipomatous)>60/F: 2NAEMA: (+), S-100: (+), PR: (+)M1B1: < 5% (n = 2)
Savardekar et al., 2016211 (lipomatous)44/FAsymptomatic/FU: 1 yrNANA
Jaiswal et al., 2011365 (lipomatous): 4 (meningothelial), 1 (transitional)(17–45)/F: 1, M: 4NRs/FU: 6–34 mos (mean 20.8 mos)NANA
Kim et al., 201541 (intraosseous lipomatous)49/MNAS-100: (+), PR: (+)Ki-67: < 0.5%
Gasparinho et al., 2015221 (lipomatous)49/FNAEMA: (+), vimentin: (+), S-100: (±), PR: (+) in meningothelial cells but not adipocyte-like cellsKi-67: 5%
Yüksel et al., 201751 (lipomatous)77/MNAEMA: (+), vimentin: (+), PR: (+), S-100: (–), GFAP: (–)Ki-67: 1–2%
Carlotti Júnior et al., 1998231 (lipoblastic)51/MNAEMA: (+), vimentin: (+), S-100: (+), GFAP (–)NA
Radwan et al., 2016241 (lipomatous)58/FNR/FU: 1 moNANA
Lattes and Bigotti, 1991257 (lipoblastic)(36–90)/F: 2, M: 5NRs/FU: 6–18 mosEMA: (+) n = 1, vimentin: (+) n = 3, S-100: (+) n = 2, (±) n = 1, GFAP: (–) n = 3NA
Liebig et al., 1998261 (lipomatous secretory)67/FNAKiM1P: (+), cytokeratin: (+), PR: (+)NA
de Eulate-Beramendi et al., 2019271 (lipomatous)42/MNR & asymptomatic/FU: 3 yrsNANA
Harmouch et al., 2005282 (lipomatous)NANAEMA: (+), PR: (+)NA
LeRoux et al., 1989291 (lipomatous)61/FNANANA
Fitt et al., 1996301 (lipomatous)78/MNAOil Red O: (+)NA
Kimiwada et al., 2004311 (lipomatous)70/FNAEMA: (+), vimentin: (+), S-100: (–), Oil Red O: (+)Ki-67: 2.8%
Kashimura et al., 2008321 (lipomatous)55/MNANANA
Kasantikul and Brown, 1984331 (lipomatous)69/FNR/FU: 1 yrNANA
Patil et al., 2017341 (secretory w/ lipomatous components)40/FNAEMA: (+), vimentin: (+), Oil Red O: (+)NA
Matyja et al., 2005351 (secretory w/ lipomatous components)58/FNAEMA: (+), CEA: (+), Oil Red O: (+)NA

CEA = carcinoembryonic antigen; FU = follow-up; GFAP = glial fibrillary acidic protein; NA = not available; NR = no recurrence; PR = progesterone receptor; SMA = smooth muscle actin; + = positive staining; − = negative staining; ± = some regions with positive staining and other regions with negative staining.

Terminology used by authors was used to classify cases in parentheses.

Positive S-100 staining is in adipocyte-like cells only and not meningothelial cells unless noted otherwise.

Similar to most other types of meningioma, the symptoms of lipomatous meningioma vary according to the size and location of the tumor and are more often found in females than males (females:males = 2:1). The most common symptoms reported by patients with lipomatous meningioma are seizures (36%) and headaches (34%); other less common symptoms include visual disorders, hemiparesis, gait instability, or behavioral abnormalities.6 Since clinical presentation alone is not sufficient to differentiate lipomatous meningioma from other subtypes, radiological and histological findings are necessary to obtain a definitive diagnosis. As mentioned previously, MRI and CT are the imaging modalities most often used to diagnose meningiomas and may even be used to identify certain lipomatous features. The attenuation coefficient of fat is –50 to –100 Hounsfield units (HU), permitting identification of lipid accumulation in tumors through hyperintense signals on T1W and T1W MRI or hypodense signals on CT.23,36 However, a limitation of radiological imaging is that it may be difficult to distinguish lipomatous meningioma, or meningiomas in general, from other meningeal neoplasms such as solitary fibrous tumor (SFT)/hemangiopericytoma. This is an important distinction to make because SFTs are often malignant and have a greater likelihood of recurrence and metastasis compared with meningiomas, thus potentially requiring adjuvant radiotherapy or chemotherapy.37 SFTs can be identified immunohistochemically from other, less aggressive tumors through the expression of STAT6, which was negative in our case, and in other lipomatous meningiomas in the literature.38 Additionally, the presence of adipose tissue alone may not be sufficient for diagnosis and IHC is often required to further narrow the diagnosis. For instance, lipoma/liposarcoma can be differentiated from lipomatous meningioma by the presence of EMA in the latter but absence of the former.6,39 In xanthomatous meningioma, lipidized cells contain vacuolated, lipid-filled cytoplasm and centrally placed nuclei consisting mainly of cholesterol,40 whereas lipomatous meningiomas have peripherally placed nuclei, composed of triglycerides.36 Furthermore, as is suggestive of the clinically benign nature of lipomatous meningiomas, the proliferative indexes in these cases are often extremely low (Ki-67/MIB-1 of < 1%–2%),4,5,16 whereas they are comparatively elevated in lipoma (MIB-1 index ∼ 5%)41 and liposarcoma (MIB-1 index ∼ 20%).39 Some other differential diagnoses to also consider include chondroma, metastatic mucinous carcinomas, giant cell glioblastomas, and epidermoid cysts.6 As is the case for most other symptomatic meningiomas, maximal safe resection is the preferred treatment approach for lipomatous meningioma.6

Observations

Lipomatous meningioma is a rare subtype of metaplastic meningioma, with recent studies suggesting that the presence of adipose-like cells is a result of metabolic alterations resulting in lipid accumulation rather than true metaplasia.15 This patient had a tumor located in the right posterior fossa, in the cerebellar convexity and had a history of migraines and headaches associated with nausea. On T1W/T2W MRI, lipomatous features of meningioma often present with hyperintensity, and thus can present as heterogenous enhancement patterns depending on the fat content and distribution within the tumor.42 In our case, the axial T1W MRI showed hyperintensity with some heterogeneity (Fig. 1). Positive EMA staining can be used to confirm tumor status and differentiate from other potential mimickers such as lipoma and liposarcoma.6,39,41 Negative STAT6 staining can be used to distinguish these tumors from hemangiopericytomas.38(p6) The specimen in our case was both EMA positive and STAT6 negative.

Lessons

A limitation of grading tumors based on histopathological classification alone is that there may be interrater variability and ambiguity with the specific criteria that confirm a given diagnosis.8 Molecular characterization may supplement histopathology by providing a more robust, unique signature that can definitively differentiate lipomatous meningiomas from other tumor subtypes. One notable approach involves DNA methylation–based classification in which methylation profiles can be used in combination with machine-learning algorithms to determine tumor pathology and predict clinical progression more accurately. Capper et al.12 found that diagnosis may change in up to 12% of cases when using DNA methylation compared with just histopathological grading. We conducted the first molecular characterization of a lipomatous meningioma case and confirmed that lipomatous meningioma is a unique subtype of meningioma, highly benign in nature, and includes unique copy number variations (CNVs) such as loss of SMARCB1 and early loss of chromosome 8 that are not typically found in other meningioma subtypes. Although loss of NF2 is unsurprising in meningioma, SMARCB1 deletions co-occurring with NF2 mutations are rare and more often found in atypical, higher grade meningiomas or in familial meningiomas.43 The loss of FGFR1/TACC1, MYBL1, and MYC on chromosome 8 and gains of CNVs on chromosome 7 and 14q (Fig. 3B) are rarely seen in meningiomas, so the presence of these alterations in lipomatous meningioma may be related to its unique pathogenesis.44 In breast cancer, loss of chromosome 8p was found to relate to aberrant fat metabolism—specifically, upregulation of 18 genes involved in the conversion of acetyl-CoA to cholesterol and fatty acids.45 Future studies are needed to investigate whether similar loss of chromosome 8p in lipomatous meningioma and other underlying alterations in tumor fat metabolism could explain the pathogenesis of lipomatous meningiomas. Our study was limited in that DNA methylation profiling was completed on only a single case. These findings would need to be corroborated with a larger cohort to validate whether these methylation changes and CNVs could be consistently identified. In addition, genetic and epigenetic changes would also have to be compared with transcriptomic and proteomic findings to obtain a more thorough biological characterization and determine if these meningiomas classify into any other known molecular groups. Although extremely rare, differentiating lipomatous meningioma from other, more aggressive meningioma subtypes or SFT, through both histopathology and molecular alterations, is important because it may alter management plans clinically and prevent unnecessary interventions such as radiotherapy following surgery. Moreover, this case provides an interesting entity of study of a uniquely benign subtype of meningioma, which may be important in understanding the biological determinants of the aggressiveness of these tumors.

Acknowledgments

This work was supported by the Mach-Gaensslen Foundation of Canada.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Patel, Wang, Merali, Nassiri. Acquisition of data: Patel, Wang, Merali, Wei. Analysis and interpretation of data: Patel, Wang, Merali, Patil, Sosa. Drafting of the article: Patel. Critically revising the article: Patel, Wang, Merali, Nassiri, Coire. Reviewed submitted version of the manuscript: Patel, Nassiri, Sosa, Coire, Zadeh. Approved the final version of the manuscript on behalf of all authors: Patel. Statistical analysis: Sosa, Zadeh. Study supervision: Wang, Zadeh.

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  • 17

    Yamada H, Hanada T, Okuda S, Yokota A, Haratake J. Secretory meningioma with lipomatous component: case report. Brain Tumor Pathol. 1999;16(2):7780.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Withers T, Klevansky A, Weinstein SR. Lipomeningioma: case report and review of the literature. J Clin Neurosci. 2003;10(6):712714.

  • 19

    Mariniello G, Spaziante R, Del Basso De Caro ML, de Divitiis E. An unusual case of lipoblastic meningioma of the falx cerebri. Clin Neurol Neurosurg. 2000;102(3):180185.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Colnat-Coulbois S, Kremer S, Weinbreck N, Pinelli C, Auque J. Lipomatous meningioma: report of 2 cases and review of the literature. Surg Neurol. 2008;69(4):398402, discussion 402.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Savardekar AR, Verma A, Narayan V, Mahadevan A, Rao MB. Pathological correlation of magnetic resonance imaging features in a classical case of lipomatous meningioma. Surg Neurol Int. 2016;7:32.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Gasparinho MG, Ferreira M, Lavrador JP, Livraghi S. Revisiting lipomatous meningioma: a case report and review of an unusual entity. Int J Surg Pathol. 2015;23(5):399403.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Carlotti Júnior CG, Colli BO, Chimelli L, Dos Santos AC, Elias Júnior J. Lipoblastic meningioma. Case report. Arq Neuropsiquiatr. 1998;56(3B):661665.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Radwan W, Lucke-Wold B, Cheyuo C, Ahn J, Gyure K, Bhatia S. Lipomatous meningioma: case report and review of the literature. Case Stud Surg. 2016;2(4):5861.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Lattes R, Bigotti G. Lipoblastic meningioma: “vacuolated meningioma”. Hum Pathol. 1991;22(2):164171.

  • 26

    Liebig T, Hoffmann T, Hosten N, et al. Lipomatous secretory meningioma: case report and review of the literature. Neuroradiology. 1998;40(10):656658.

  • 27

    de Eulate-Beramendi SA, Piña-Batista KM, Rial-Basalo JC. Extradural en-plaque spinal lipomatous meningioma: a case report and literature review. Surg Neurol Int. 2019;10:49.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Harmouch T, Colombat M, El Amri A, et al. [Lipomatous meningioma: two case reports]. Ann Pathol. 2005;25(5):389392.

  • 29

    LeRoux P, Hope A, Lofton S, Harris AB. Lipomatous meningioma—an uncommon tumor with distinct radiographic findings. Surg Neurol. 1989;32(5):360365.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Fitt GJ, Kalnins R, Mitchell LA. Lipomatous meningioma: characteristic computed tomographic appearance. Australas Radiol. 1996;40(1):8487.

  • 31

    Kimiwada T, Motohashi O, Kumabe T, Watanabe M, Tominaga T. Lipomatous meningioma of the brain harboring metastatic renal-cell carcinoma: a case report. Brain Tumor Pathol. 2004;21(1):4752.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Kashimura H, Arai H, Ogasawara K, Beppu T, Kurose A, Ogawa A. Lipomatous meningioma with concomitant acute subdural hematoma—case report. Neurol Med Chir (Tokyo). 2008;48(10):466469.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Kasantikul V, Brown WJ. Lipomatous meningioma associated with cerebral vascular malformation. J Surg Oncol. 1984;26(1):3539.

  • 34

    Patil PR, Warpe BM, Juvekar VH, Manohar V. Meningioma with the unique coexistence of secretory and lipomatous components: a case report with immunohistochemical study. Indian J Pathol Microbiol. 2017;60(3):381384.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Matyja E, Naganska E, Zabek M, Jagielski J. Meningioma with the unique coexistence of secretory and lipomatous components: a case report with immunohistochemical and ultrastructural study. Clin Neuropathol. 2005;24(6):257261.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Jaiswal AK, Mehrotra A, Kumar B, et al. Lipomatous meningioma: a study of five cases with brief review of literature. Neurol India. 2011;59(1):8791.

  • 37

    Rutkowski MJ, Jian BJ, Bloch O, et al. Intracranial hemangiopericytoma: clinical experience and treatment considerations in a modern series of 40 adult patients. Cancer. 2012;118(6):16281636.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Doyle LA, Vivero M, Fletcher CD, Mertens F, Hornick JL. Nuclear expression of STAT6 distinguishes solitary fibrous tumor from histologic mimics. Mod Pathol. 2014;27(3):390395.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Fanburg-Smith JC, Miettinen M. Liposarcoma with meningothelial-like whorls: a study of 17 cases of a distinctive histological pattern associated with dedifferentiated liposarcoma. Histopathology. 1998;33(5):414424.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Ishida M, Fukami T, Nitta N, et al. Xanthomatous meningioma: a case report with review of the literature. Int J Clin Exp Pathol. 2013;6(10):22422246.

  • 41

    Fuga M, Tanaka T, Yamamoto Y, Hasegawa Y, Murayama Y, Takahashi-Fujigasaki J. Lipoma in the corpus callosum presenting with epileptic seizures associated with expanding perifocal edema: a case report and literature review. Case Rep Neurol Med. 2015;2015:520208.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42

    O’Leary S, Adams WM, Parrish RW, Mukonoweshuro W. Atypical imaging appearances of intracranial meningiomas. Clin Radiol. 2007;62(1):1017.

  • 43

    Harmancı AS, Youngblood MW, Clark VE, et al. Integrated genomic analyses of de novo pathways underlying atypical meningiomas. Nat Commun. 2017;8(1):14433.

  • 44

    Maas SLN, Stichel D, Hielscher T, et al. Integrated molecular-morphologic meningioma classification: a multicenter retrospective analysis, retrospectively and prospectively validated. J Clin Oncol. 2021;39(34):38393852.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45

    Cai Y, Crowther J, Pastor T, et al. Loss of chromosome 8p governs tumor progression and drug response by altering lipid metabolism. Cancer Cell. 2016;29(5):751766.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand
  • FIG. 1.

    A: Preoperative axial cranial T1W MRI without gadolinium showing a hyperintense, heterogeneous, extra-axial lesion in the right cerebellar convexity. B: Preoperative sagittal cranial T2W MRI demonstrating a cerebrospinal fluid cleft and some adjacent perilesional edema. C: Postoperative axial cranial CT demonstrating complete macroscopic resection of this mass.

  • FIG. 2.

    Histopathological microscopic imaging of the lipomatous meningioma case. Each image is 8× the original magnification with a 20× image embedded within. A: H&E staining illustrates meningothelial cell morphology and mature adipocyte-like cells with flattened, peripherally placed nuclei. B: EMA cytoplasmic immunostaining is positive. C: STAT6 nuclear immunostaining is negative.

  • FIG. 3.

    DNA methylation profiling of lipomatous meningioma. A: DKFZ classifier v12.5 diagnosis class and meningioma subclasses with their respective calibrated score. A calibrated score > 0.8 is required to classify this as a “match.” B: Copy number plot demonstrating gains and losses of chromosome arms from 1 to 22 as well as specific annotated gene loci on these arms. Gains/amplification (green) represent positive deviation and losses (red) represent negative deviation from baseline. Twenty-nine brain tumor relevant gene regions are highlighted. C: A t-distributed stochastic neighbor embedding plot (t-SNE) plot depicting clustering of lipomatous meningioma (red asterisk) most closely with meningioma reference cases (blue) from the DKFZ classifier v11.4. D: Quality-control profile from DNA methylation analysis performed prior to DNA methylation profiling for recurrence risk demonstrating distribution of genome-wide methylation values (Beta) for this sample. E: Tumor recurrence risk using DNA methylation–based recurrence prediction from tumor methylome alone (agnostic to WHO grade and other clinical features) (above) and based on the clinical nomogram published by Nassiri et al.13 A IDH = IDH glioma, subclass astrocytoma; ANA PA = anaplastic pilocytic astrocytoma; ATRT = atypical teratoid/rhabdoid tumor; CHGL = chordoid glioma of the third ventricle; CHORDM = chordoma; CN = central neurocytoma; CNS NB = central nervous system neuroblastoma; CONTR = control tissue; CPH = craniopharyngioma; DLGNT = diffuse leptomeningeal glioneuronal tumor; DMG = diffuse midline glioma; HGNET = high grade neuroepithelial tumor; HMB = hemangioblastoma; IHG = infantile hemispheric glioma; LGG = low grade glioma; LIPN = liponeurocytoma; LYMPHO = lymphoma; MB = medulloblastoma; MC = methylation class; MELAN = melanoma; MELCYT = melanocytoma; MNG = meningioma; O IDH = IDH glioma; subclass 1p/19q co-deleted oligodendroglioma; PGG = paraganglioma; PIN T = pineoblastoma; PITAD = pituitary adenoma; PITUI = pituicytoma; PLASMA = plasmacytoma; PLEX = plexus tumor; PTPR = papillary tumor of the pineal region; PXA = pleomorphic xanthoastrocytoma; RETB = retinoblastoma; SCHW = schwannoma; SFT HMPC = solitary fibrous tumor/hemangiopericytoma; SUBEPN = supendymoma.

  • 1

    Buerki RA, Horbinski CM, Kruser T, Horowitz PM, James CD, Lukas RV. An overview of meningiomas. Future Oncol. 2018;14(21):21612177.

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    Lapolla P, Familiari P, Zancana G, et al. Lipomatous meningioma: clinical-pathological findings, imaging characterisation and correlations of a rare type of meningioma. In Vivo. 2021;35(6):30313037.

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    Menke JR, Raleigh DR, Gown AM, Thomas S, Perry A, Tihan T. Somatostatin receptor 2a is a more sensitive diagnostic marker of meningioma than epithelial membrane antigen. Acta Neuropathol. 2015;130(3):441443.

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    Attems J, Toledo JB, Walker L, et al. Neuropathological consensus criteria for the evaluation of Lewy pathology in post-mortem brains: a multi-centre study. Acta Neuropathol. 2021;141(2):159172.

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    Sahm F, Schrimpf D, Stichel D, et al. DNA methylation-based classification and grading system for meningioma: a multicentre, retrospective analysis. Lancet Oncol. 2017;18(5):682694.

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    Nassiri F, Chakravarthy A, Feng S, et al. Detection and discrimination of intracranial tumors using plasma cell-free DNA methylomes. Nat Med. 2020;26(7):10441047.

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    Choudhury A, Magill ST, Eaton CD, et al. Meningioma DNA methylation groups identify biological drivers and therapeutic vulnerabilities. Nat Genet. 2022;54(5):649659.

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    Capper D, Jones DTW, Sill M, et al. DNA methylation-based classification of central nervous system tumours. Nature. 2018;555(7697):469474.

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    Nassiri F, Mamatjan Y, Suppiah S, et al. DNA methylation profiling to predict recurrence risk in meningioma: development and validation of a nomogram to optimize clinical management. Neuro Oncol. 2019;21(7):901910.

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    Capper D, Stichel D, Sahm F, et al. Practical implementation of DNA methylation and copy-number-based CNS tumor diagnostics: the Heidelberg experience. Acta Neuropathol. 2018;136(2):181210.

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    Roncaroli F, Scheithauer BW, Laeng RH, Cenacchi G, Abell-Aleff P, Moschopulos M. Lipomatous meningioma: a clinicopathologic study of 18 cases with special reference to the issue of metaplasia. Am J Surg Pathol. 2001;25(6):769775.

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  • 16

    Tang H, Sun H, Chen H, et al. Clinicopathological analysis of metaplastic meningioma: report of 15 cases in Huashan Hospital. Chin J Cancer Res. 2013;25(1):112118.

    • PubMed
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  • 17

    Yamada H, Hanada T, Okuda S, Yokota A, Haratake J. Secretory meningioma with lipomatous component: case report. Brain Tumor Pathol. 1999;16(2):7780.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 18

    Withers T, Klevansky A, Weinstein SR. Lipomeningioma: case report and review of the literature. J Clin Neurosci. 2003;10(6):712714.

  • 19

    Mariniello G, Spaziante R, Del Basso De Caro ML, de Divitiis E. An unusual case of lipoblastic meningioma of the falx cerebri. Clin Neurol Neurosurg. 2000;102(3):180185.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 20

    Colnat-Coulbois S, Kremer S, Weinbreck N, Pinelli C, Auque J. Lipomatous meningioma: report of 2 cases and review of the literature. Surg Neurol. 2008;69(4):398402, discussion 402.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Savardekar AR, Verma A, Narayan V, Mahadevan A, Rao MB. Pathological correlation of magnetic resonance imaging features in a classical case of lipomatous meningioma. Surg Neurol Int. 2016;7:32.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Gasparinho MG, Ferreira M, Lavrador JP, Livraghi S. Revisiting lipomatous meningioma: a case report and review of an unusual entity. Int J Surg Pathol. 2015;23(5):399403.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Carlotti Júnior CG, Colli BO, Chimelli L, Dos Santos AC, Elias Júnior J. Lipoblastic meningioma. Case report. Arq Neuropsiquiatr. 1998;56(3B):661665.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Radwan W, Lucke-Wold B, Cheyuo C, Ahn J, Gyure K, Bhatia S. Lipomatous meningioma: case report and review of the literature. Case Stud Surg. 2016;2(4):5861.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Lattes R, Bigotti G. Lipoblastic meningioma: “vacuolated meningioma”. Hum Pathol. 1991;22(2):164171.

  • 26

    Liebig T, Hoffmann T, Hosten N, et al. Lipomatous secretory meningioma: case report and review of the literature. Neuroradiology. 1998;40(10):656658.

  • 27

    de Eulate-Beramendi SA, Piña-Batista KM, Rial-Basalo JC. Extradural en-plaque spinal lipomatous meningioma: a case report and literature review. Surg Neurol Int. 2019;10:49.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Harmouch T, Colombat M, El Amri A, et al. [Lipomatous meningioma: two case reports]. Ann Pathol. 2005;25(5):389392.

  • 29

    LeRoux P, Hope A, Lofton S, Harris AB. Lipomatous meningioma—an uncommon tumor with distinct radiographic findings. Surg Neurol. 1989;32(5):360365.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Fitt GJ, Kalnins R, Mitchell LA. Lipomatous meningioma: characteristic computed tomographic appearance. Australas Radiol. 1996;40(1):8487.

  • 31

    Kimiwada T, Motohashi O, Kumabe T, Watanabe M, Tominaga T. Lipomatous meningioma of the brain harboring metastatic renal-cell carcinoma: a case report. Brain Tumor Pathol. 2004;21(1):4752.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Kashimura H, Arai H, Ogasawara K, Beppu T, Kurose A, Ogawa A. Lipomatous meningioma with concomitant acute subdural hematoma—case report. Neurol Med Chir (Tokyo). 2008;48(10):466469.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Kasantikul V, Brown WJ. Lipomatous meningioma associated with cerebral vascular malformation. J Surg Oncol. 1984;26(1):3539.

  • 34

    Patil PR, Warpe BM, Juvekar VH, Manohar V. Meningioma with the unique coexistence of secretory and lipomatous components: a case report with immunohistochemical study. Indian J Pathol Microbiol. 2017;60(3):381384.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 35

    Matyja E, Naganska E, Zabek M, Jagielski J. Meningioma with the unique coexistence of secretory and lipomatous components: a case report with immunohistochemical and ultrastructural study. Clin Neuropathol. 2005;24(6):257261.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 36

    Jaiswal AK, Mehrotra A, Kumar B, et al. Lipomatous meningioma: a study of five cases with brief review of literature. Neurol India. 2011;59(1):8791.

  • 37

    Rutkowski MJ, Jian BJ, Bloch O, et al. Intracranial hemangiopericytoma: clinical experience and treatment considerations in a modern series of 40 adult patients. Cancer. 2012;118(6):16281636.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 38

    Doyle LA, Vivero M, Fletcher CD, Mertens F, Hornick JL. Nuclear expression of STAT6 distinguishes solitary fibrous tumor from histologic mimics. Mod Pathol. 2014;27(3):390395.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 39

    Fanburg-Smith JC, Miettinen M. Liposarcoma with meningothelial-like whorls: a study of 17 cases of a distinctive histological pattern associated with dedifferentiated liposarcoma. Histopathology. 1998;33(5):414424.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 40

    Ishida M, Fukami T, Nitta N, et al. Xanthomatous meningioma: a case report with review of the literature. Int J Clin Exp Pathol. 2013;6(10):22422246.

  • 41

    Fuga M, Tanaka T, Yamamoto Y, Hasegawa Y, Murayama Y, Takahashi-Fujigasaki J. Lipoma in the corpus callosum presenting with epileptic seizures associated with expanding perifocal edema: a case report and literature review. Case Rep Neurol Med. 2015;2015:520208.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 42

    O’Leary S, Adams WM, Parrish RW, Mukonoweshuro W. Atypical imaging appearances of intracranial meningiomas. Clin Radiol. 2007;62(1):1017.

  • 43

    Harmancı AS, Youngblood MW, Clark VE, et al. Integrated genomic analyses of de novo pathways underlying atypical meningiomas. Nat Commun. 2017;8(1):14433.

  • 44

    Maas SLN, Stichel D, Hielscher T, et al. Integrated molecular-morphologic meningioma classification: a multicenter retrospective analysis, retrospectively and prospectively validated. J Clin Oncol. 2021;39(34):38393852.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 45

    Cai Y, Crowther J, Pastor T, et al. Loss of chromosome 8p governs tumor progression and drug response by altering lipid metabolism. Cancer Cell. 2016;29(5):751766.

    • PubMed
    • Search Google Scholar
    • Export Citation

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