Acta Neurochir (Wien) (2005) 147: 965–972 DOI 10.1007/s00701-005-0578-3
Clinical Article Microcystic meningiomas: radiological characteristics of 16 cases S. H. Paek1 , S. H. Kim1 , K. H. Chang2 , C.-K. Park1 , J. E. Kim1 , D. G. Kim1 , S.-H. Park3 , and H.-W. Jung1 1 Department of Neurosurgery and Clinical Research Institute, Seoul National University College of Medicine, Seoul National University Hospital, Seoul, Korea 2 Department of Radiology, Seoul National University College of Medicine, Seoul National University Hospital, Seoul, Korea 3 Department of Pathology, Seoul National University College of Medicine, Seoul National University Hospital, Seoul, Korea
Received March 3, 2005; accepted May 24, 2005; published online July 18, 2005 # Springer-Verlag 2005
Summary Background. As a rare subtype of meningioma, only a few reports deal with radiological characteristics of microcystic meningiomas and the problem remains controversial. The authors have analyzed the radiological findings of a series of microcystic meningiomas with a special focus on magnetic resonance images (MRI) and conventional angiography. Method. Sixteen patients of histologically proven microcystic meningiomas were included. Analysis of preoperative MRI including signal intensity characteristics, enhancement patterns and peritumoural edema were performed and correlated with angiographic and histological findings. Peritumoural edema was graded using edema index (EI) which was defined as the ratio of VE=VT. Findings. The tumours were uniformly visualized as a high-signal mass lesion in T2-weighted images and as a low-signal mass lesion in T1-weighted images regardless of tumour vascularity shown by angiography. T2-weighted images revealed that peritumoural brain edema was severe in 11, moderate in 1, mild in 2 and negligible in 2 patients and this was closely related to the co-existence of irregular tumour marginal enhancement. However, other features failed to distinguish these lesions from other subtypes of meningioma. Conclusions. The cases presented demonstrate that characteristic MRI findings suggestive of microcystic meningiomas are; (1) low signal intensity mass in T1- and high signal intensity mass in T2-weighted images; (2) high incidence of peritumoural edema. Keywords: Microcystic meningioma; peritumoural edema; radiological characteristics; signal intensity.
Back in 1956, Masson first described a peculiar variant of meningioma of the humid or wet form, characterized by masses of meningeal syncytium in the process of vacuolization with numerous lacunae or elongated slits and a very rich network of vessels [7]. Subsequent reports identified such characteristic clinicopathological findings of vacuolation, myxomatous change, and microcysts in certain meningiomas and designated that subgroup as a microcystic meningioma [9]. Thereafter several reports dealt with characteristics of computed tomography (CT) and=or magnetic resonance images (MRI) in microcystic meningiomas [1, 5, 8, 10, 11, 13, 14, 16]. Nishio et al. reported that microcystic meningiomas are radiologically identical to other subtypes [11]. While Shimoji et al. found characteristic neuroimaging indications of this rare variant [16]. However, these investigations of previous reports are on the basis of small numbers or sporadic cases. The authors here report the radiological findings of microcystic meningioma in a series of 16 cases with a special focus on MRI and conventional angiography.
Materials and methods Introduction Microcystic meningioma was originally classified as a subtype of meningioma by the World Health Organization classification of brain tumours in 1993 [4, 15]. It accounts for 1.6% of intracranial meningiomas [4, 6].
Between October 1995 and April 2004, a total of 915 tumours were histologically diagnosed as benign meningioma after surgery at our institute. Among them, 16 tumours were proven to be of the microcystic subtype. The median age of the patients was 59 years (range: 38– 71 years) with a male to female ratio of 5:11. In 11 patients, tumours originated from convexity meninges and in 5 from falx meninges.
Sex
M
F
F F F M
F F
M M
M
F
F F
F F
No.
1
2
3 4 5 6
7 8
9 10
11
12
13 14
15 16
54 64
48 52
56
49
61 59
67 62
63 71 67 37
38
47
Age
weakness headache dysarthria seizure headache seizure headache weakness headache dizziness headache visual disturbance headache headache
headache visual disturbance weakness weakness weakness weakness
headache
Symptom
convexity convexity
convexity falx
convexity
convexity
convexity convexity
convexity convexity
falx convexity convexity falx
falx
falx
Location
– iso
– –
–
low
– low
– –
– – – low
–
iso
– –
– –
peripheral enhancement –
– –
– – – peripheral enhancement – –
homogenous enhancement –
homogenous heterogeneous
heterogeneous homogenous
homogenous
heterogeneous
homogenous homogenous
homogenous peripheral
homogenous homogenous homogenous peripheral
homogenous
homogenous
Enhancement
Pre-contrast
Contrast
MRI
CT
Table 1. Summary of characteristics of 16 patients with microcystic meningioma
yes yes
yes yes
yes
yes
yes yes
yes yes
yes yes yes yes
yes
yes
Dural tail sign
31.9 108.1
42.4 19.8
18.4
23.3
13.5 28.8
31.8 38.8
29.5 33.5 40.1 45.5
30.5
21.4
Tumor volume (cm3 )
211.4 0
292.0 8.2
110.7
86.6
99.5 15.9
113.1 0
120.4 212.0 111.8 86.4
214.3
152.4
Edema volume (cm3 )
6.6 0
6.8 0.4
6.0
3.7
7.4 0.5
3.6 0
4.0 6.3 2.7 1.9
7.0
7.1
Edema index
severe negligible
severe mild
severe
severe
severe mild
severe negligible
severe severe severe moderate
severe
severe
Edema
no no
yes yes
yes
no
yes yes
yes yes
no yes no no
no
no
Hyperostosis
disrupted intact
disrupted disrupted
disrupted
disrupted
disrupted disrupted
disrupted intact
disrupted disrupted disrupted disrupted
disrupted
disrupted
Aranchnoid plane
dual (equal) dual (equal)
dual (pial) dual (equal)
–
dual (dural)
dual (dural) dual (dural)
dual (dural) avascular
dual (dural) – dual (equal) avascular
dual (pial)
dual (pial)
Tumor supply (dominancy)
Angiography
966 S. H. Paek et al.
Microcystic meningiomas: radiological characteristics of 16 cases MRI was performed in all patients before surgery on a 1.5 tesla MRI unit in 10 patients and on a 1.0 tesla MRI unit in 6 patients. Precontrast T1-weighted sagittal and/or axial images and T2-weighted axial images were obtained in all patients. Contrast enhanced T1-weighted images
967 were obtained with intravenous injection of Gd-DTPA (gadoliniumdiethylene-triamine-penta-acetic acid) (0.1 mg=kg body weight). Slice thickness=gap was 5–7 mm=0.6–1.9 mm, the field of view 9 to 21 cm, with an acquisition matrix of 256 256. The number of excitations
Fig. 1. T2-weighted MRI of 16 patients with microcystic meningioma. The tumours are characteristically observed as a high-signal mass lesion in all cases. Note existence of predominant peritumoural edema except 2 cases (‘’ marked)
968 ranged from 2 to 3 for T1-weighted images and from 1 to 3 for T2weighted images. The peritumoural brain edema was estimated, as previously described in the author’s work [12]. Briefly, the volume of edema (VE) surrounding meningioma was estimated by measuring the volume of the high signal intensity area around the tumour mass in T2-weighted images. Tumour volume (VT) was also measured in gadolinium-enhanced T1-weighted images. The volumes were determined by using the volumetric program (Osiris+). The error associated with repeat measurements of the volume of the same MRI was within 2%. The edema index (EI) was defined as the ratio of VE=VT. The grading of edema was defined according to EI: absent or negligible (EI < 0.1); mild (0.1 < EI < 1.0); moderate (1.0 < EI < 2.0); severe (EI > 2.0). Conventional angiography and CT scan were done in 10 and 4 patients respectively. Craniotomy with gross total resection (GTR) of the tumour was performed in all cases. One patient with remarkably high vascular
S. H. Paek et al. mass underwent whole brain radiation therapy before surgery for the purpose of reduction of vascularity. Histopathological investigation was undertaken by the neuropathologist (SHP). Histological characteristics including MIB-1 and Ki-67 index labelling were carefully correlated with imaging studies.
Results Clinical and radiological characteristics of all patients are summarized in Table 1. The CT scan of 5 patients revealed iso-density or low-density mass lesions in precontrast images and diverse patterns of contrast enhancement. In MRI, all 16 tumours were observed
Fig. 2. Case 15. The mass lesion appears as a low signal in the T1-weighted MRI with strong homogeneous enhancement after gadolinium injection. Severe peritumoural brain edema is visible. External and internal carotid angiography reveals profuse tumour staining by dual tumour supply vessels from pia and dura
Microcystic meningiomas: radiological characteristics of 16 cases
as low-signal mass lesions in T1-weighted images, while T2-weighted images showed high-signal mass lesions (Fig. 1). The tumour was densely enhanced by GdDTPA in 14 patients. Homogeneous enhancement was observed in 11 patients and heterogeneous enhancement in 3 patients. The other 2 patients showed only scanty peripheral rim enhancement. Such findings were well matched by the vascularity of tumours shown by angiog-
969
raphy in 14 patients. Angiographies of patients, who showed distinct enhancement of the tumour in MRI demonstrated strong tumour staining by the dual blood supplies from both pial and dural feeders with variable feeder dominancy (Fig. 2). In contrast, the tumour was rarely enhanced by Gd-DTPA in 2 patients, in whom angiography demonstrated avascularity of the tumour (Fig. 3). Peritumoural brain edema was observed in 14
Fig. 3. Case 8. The low signal mass lesion in the T1-weighted MRI remains non-enhanced for the most part with only scanty thin peripheral enhancement after gadolinium injection. Peritumoural edema is absent in this case. Both external and internal carotid angiography reveals no tumour staining
970
(87.5%) patients. The degree of peritumoural brain edema analyzed in T2-weighted images was severe in 11, moderate in 1 and mild in 2. Radiologically, peritumoural edema was closely related to the existence of irregular marginal tumour enhancement which implied disruptions of the arachnoid membrane (Fig. 4). T1weighted images with Gd-DTPA demonstrated enhancement of the dura adjacent to the tumour, so called ‘‘dural
S. H. Paek et al.
tail sign’’ in all patients, whereas hyperostotic change was found in half of the patients. Histopathologically the tumours showed the pure microcystic form of meningioma in 15 cases and a mixed form with meningotheliomatous meningioma in one case (case 16). They showed vacuolated or microcystic appearances which were intercellular or intracytoplasmic. Whorls and psammoma bodies were rare. Generally, blood vessels were abundant and frequently showed considerable vascular hyalinization (Fig. 5). The tumour cells show large pleomorphic or hyperchromatic nuclei, but most of these nuclei were negative for MIB-1. Overall Ki-67 labelling indices were low (less than 1%) except one case (2.5%). Thus we failed to find any correlations between mitosis index and imaging features.
Discussion
Fig. 4. Heterogeneously enhanced mass with severe peritumoural edema. Note mottled irregular marginal tumour enhancement implying disrupted arachnoid membrane (arrowheads)
Fig. 5. Histological features of the tumour. Microcystic meningioma shows variable sized cystic spaces and=or vacuolated cytoplasm with rich hyalinized blood vessels (H&E100)
The MRI appearances of meningiomas according to subtypes are various and controversial. Kaplan et al. suggested characteristic MRI findings differentiating subtypes of meningiomas from one another [3]. However, their experiences are limited to only 4 subtypes (meningothelial, transitional, fibroblastic, and angioblastic) and showed unpredictable signal intensities of the tumour along with subtypes. In the present series, however, all the cases uniformly demonstrated hypointensity in T1-weighted images and hyperintensity in T2-weighted images. These were also consistent features in the previously reported cases [1, 5, 8, 11, 16]. However, any other features of the tumour in MRI failed to show characteristics distinguishable from other subtypes. Bromley et al. reported a case of microcystic meningioma with CT findings [1]. A pre-contrast CT scan revealed a large hypodense mass with surrounding edema in the right frontal lobe. With contrast injection, the tumour was densely and homogeneously enhanced. Nishio et al. reported 6 cases of microcystic meningiomas with clinical and neuro-imaging features [11]. They reported that the CT scans showed an iso-density mass in 3, low-density mass in 2, and high-density mass in one. And all tumours demonstrated homogeneous contrast enhancement with peritumoural edema. There were several reports focusing on characteristic radiological findings of microcystic meningioma. Kubota et al. reported a case of a non-enhancing microcystic meningioma with CT and MRI findings [5]. The CT scan revealed a hypodense mass in the right cerebello-pontine angle with slight enhancement after contrast injection.
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Microcystic meningiomas: radiological characteristics of 16 cases
MRI demonstrated a large mass with a high signal in T2-weighted images and a low-signal with slight enhancement in T1-weighted images. Shimoji et al. also reported a case of microcystic meningioma featuring similar imaging characteristics [16]. They observed a slightly high density mass in the right frontal convexity with heterogeneous contrast enhancement in CT. And the same mass revealed a hypo-intense lesion with faint reticular enhancement in T1-weighted MRI. They suggested that the degenerative character of the tumour may be reflected by its poor enhancement on CT and MRI. Although these reports indicated that the faint enhancement of the mass might be a radiological characteristic of microcystic meningioma, our data showed that these patterns are restricted to only minor cases of microcystic meningioma. The majority of microcystic meningioma showed dense enhancement and this was well correlated with angiographic findings of a profuse dual blood supply from both pial and dural feeders. Therefore, the degree of vascularity shown in angiography was thought to determine the enhancement pattern on MRI. Histological evidence of abundant blood vessels found in most of the cases also supported these findings. Thus the enhancement pattern was thought to fail to characterize microcystic meningiomas. Another characteristic MRI finding of microcystic meningioma was the high incidence of severe peritumoural brain edema compared to that of usual meningioma. The development of peritumoural edema occurs in 40–60% of meningiomas [18]. In the present series, peritumoural edema was observed in 87.5%. Moreover, the majority of them had developed to a severe degree. It is well known that substantial peritumoural brain edema is occasionally observed even for very small meningiomas. However, little is known about the underlying mechanism of severe peritumoural brain edema in meningioma. Yoshioka et al. suggested that vascular endothelial growth factor (VEGF) expression contributes to peritumoural brain edema formation in meningioma only if a cerebral-pial supply exists [18]. Paek et al. reported that meningioma with severe peritumoural brain edema express high levels of VEGF=vascular permeability factor (VPF) [12]. Christov et al. reported microcystic meningioma had the highest vessel density and the highest proportion of VEGF=VPF [2]. Tamiya et al. analyzed factors causing peritumoural brain edema for 125 patients with primary intracranial meningiomas [17]. They reported that cortical penetration, as defined by the disappearance of the arachnoid layer in MRI, and vascular supplies from the pial-cortical arteries in angi-
ography were significant association factors for peritumoural brain edema. These findings were also well demonstrated in the present series. Of 12 patients, whose angiograms demonstrated a dual blood supply to the tumour from both pial and dural feeders, 9 patients experienced severe peritumoral edema, mild in 2, and negligible in 1 patient. In patients with severe to moderate peritumoural brain edema, T2-weighted images demonstrated discontinuity of the CSF plane between the tumour and the brain parenchyma and T1-weighted images revealed mottled irregular enhancement beyond the tumour margin. Conclusions The cases presented demonstrate characteristic MRI findings suggestive of microcystic meningiomas namely: (1) low signal intensity mass in T1- and high signal intensity mass in T2-weighted images; (2) high incidence of peritumoural edema. It is true that these features are not unique to microcystic meningiomas. However, it could be proposed that these characteristics are also the distinctive features of other subtypes of meningiomas. Further study is necessary to discern clues about the underlying mechanism of the high incidence rate of severe peritumoural brain edema in microcystic meningiomas and find out the underlying histological basis reflecting their radiological characteristics. Acknowledgement This work was partially supported by a grant from Seoul National University Hospital, Clinical Research Institute.
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Comments Nice and well illustrated review of MRI and angiographic findings in 16 cases of microcystic meningiomas, a rare subtype morphologically characterized by cells with elongated processes loose mucinous background, giving the appearance of many small cysts. Kurt A. Jellinger Vienna This well organized paper will be of some interest to neuroradiologists and neurosurgeons, although the radiological characteristics described are not unique for this type of meningioma. In this relation, a sound comparison with the radiological features of other meningioma subtypes could be elucidating. It contains some valuable information. Hans Arnold L€ubeck
Correspondence: Dong Gyu Kim, Department of Neurosurgery, Seoul National University Hospital, 28 Yongon-dong, Chongno-gu, Seoul 110744, Korea. e-mail:
[email protected]
