Brain Tumor Pathol (2015) 32:56–60
DOI 10.1007/s10014-014-0183-3
CASE REPORT
Third ventricular atypical meningioma which recurred
with further malignant progression
Prasanna Karki • Hajime Yonezawa • Manoj Bohara •
Tatsuki Oyoshi • Hirofumi Hirano • F. M. Moinuddin •
Tsubasa Hiraki • Takako Yoshioka • Kazunori Arita
Received: 13 December 2013 / Accepted: 3 March 2014 / Published online: 20 March 2014
Ó The Japan Society of Brain Tumor Pathology 2014
Abstract Meningiomas in the third ventricle are rare,
with only very few cases reported in the literature. We
report a case of primary third ventricular anaplastic
meningioma in a 49-year-old man who presented with
progressive weakness of the left limbs and headache.
Magnetic resonance imaging revealed a tumor which
seemed to arise from the right thalamus and extending into
third ventricle. The tumor was heterogeneously enhanced
with gadolinium. It was totally removed by right transventricular-subchoroidal approach. The lesion was intraoperatively found to be whitish hard and embedded in right
thalamus, but had attachment to choroid plexus near foramen Monroi with narrow interface. The histological diagnosis was atypical meningioma, WHO Grade II. Lesion
recurred 20 months later and was resected via the same
approach, which turned out to be papillary meningioma,
WHO Grade III. The patient had second recurrence
23 months after second surgery which was operated and
the final diagnosis was anaplastic meningioma (WHO
Grade III). Literature review showed meningioma of the
P. Karki H. Yonezawa M. Bohara T. Oyoshi H. Hirano (&) F. M. Moinuddin K. Arita
Department of Neurosurgery, Graduate School of Medical and
Dental Sciences, Kagoshima University, 8-35-1 Sakuragaoka,
Kagoshima 890-8544, Japan
e-mail: [email protected]
T. Hiraki
Department of Human Pathology, Graduate School of Medical
and Dental Sciences, Kagoshima University, Kagoshima, Japan
T. Yoshioka
Department of Molecular and Cellular Pathology, Graduate
School of Medical and Dental Sciences, Kagoshima University,
Kagoshima, Japan
123
third ventricle is quite exceptional and more than half of
the cases were aggressive subtypes (Grade II or III).
Keywords Anaplastic meningioma Atypical
meningioma Papillary pattern Third ventricle
Introduction
Most meningiomas are benign and correspond to WHO
Grade I [1]. Atypical meningiomas, WHO Grade II, constitute about 15–20 % of meningiomas [2]. Papillary
meningiomas, WHO Grade III, are uncommon and comprise 1.0–2.5 % of all meningiomas [3]. Only 0.5–5 % of
the meningiomas occur in the cerebral ventricles [4] and
among intraventricular meningiomas only 16 % occur specifically in third ventricle [5]. Thus, papillary meningiomas
located within the ventricles seem unusual and those within
third ventricle seem even rarer. Anaplastic meningiomas are
relatively rare neoplasms in the central nervous system,
accounting for 1–3 % of the meningiomas [2]. They can
only be distinguished from other types of intraventricular
tumors bythe histopathological features and clinical
aggressiveness. The occurrence of meningioma in third
ventricle is itself rare and the range of transformations with
recurrences in this case is even rarer. Therefore, we present a
patient with aggressive intraventricular atypical meningioma and evaluate the pathological changes in every recurrence of tumor which leads to anaplastic transformation.
Case report
A 49-year-old man presented with progressive hemiparesis
and headache for 2 months. Non-contrast CT scan
Brain Tumor Pathol (2015) 32:56–60
57
a
b
c
d
e
f
g
h
Fig. 1 Preoperative magnetic resonance image (MRI), anatomical
exposure during the first operation and imaging of recurrent tumors.
a Axial computed tomography scan showing a lesion with mixed
density arising from right thalamus, occupying the third ventricle.
b T1-weighted MRI demonstrating an iso-intense mass in third
ventricle. c T2-weighted coronal MR image showing a lesion with
high signal intensity in third ventricle with surrounding edema. d T1weighted contrast enhanced MR image showing enhancing lesion in
third ventricle without dural attachment. e Intraoperative photograph
revealing whitish hard tumor (arrow) covered by right thalamus
(asterisk). f At the end of removal of the tumor. The last piece of the
tumor (arrow) was attached to the choroid plexus of the third
ventricle (hash). Arrow: residual part of the tumor. g T1-weighted
axial MR image showing tumor recurrence 20 months after first
surgery. h T1-weighted sagittal MR image showing tumor recurrence
23 months after second surgery
demonstrated a hyperdense lesion in the third ventricle
(Fig. 1a). Magnetic resonance imaging (MRI) revealed
bilateral enlargement of lateral ventricles and a solid tumor
arising from right thalamus reaching ventricular wall,
which was iso-intense on T1-weighted images (Fig. 1b)
and heterogeneous with peritumoral edema in right thalamus on T2-weighted images (Fig. 1c). The tumor was
heterogeneously enhanced with gadolinium (Fig. 1d).
There was no dural attachment to the tumor. On the basis
of MRI, the provisional diagnosis was glioma. The surgery
was performed through right frontal transcortical transventricular-subchoroidal approach. The whitish solid tumor
was almost entirely covered by right thalamus (Fig. 1e) but
attached to choroid plexus of third ventricle with narrow
interface (Fig. 1f). Gross total resection of the tumor was
performed in piece-meal fashion. Histopathological
examination of resected specimen revealed characteristics
of atypical meningioma according to WHO criteria for
meningioma grading [2]. The tumor comprised of meningothelial atypical cells in sheet-like growth with high
nuclear–cytoplasmic (N/C) ratio, foci of necrosis and
abundant intercellular collagen fibers (Fig. 2a). GFAP
positive islands of brain parenchyma entrapped in the
tumor were observed but the tumor tissue was negative for
GFAP (Fig. 2b). Tumor specimen showed strong, positive
staining for vimentin (Fig. 2c). Tumor specimen revealed
negative immunostaining for EMA, synaptophysin, cytokeratin and CD34. Mitotic cell count was 3 per 10 highpower fields (HPF). MIB-1 index was 8.3 % (Fig. 2d).
These findings led to the diagnosis of atypical meningioma
(WHO Grade II).
The lesion recurred after 20 months of surgery (Fig. 1g),
specimen from second surgery revealed discohesive growth
with pseudopapillae and perivascular pseudorosettes comprising majority of the tumor (Fig. 2e). The nuclei were
regular in shape and contained prominent nucleoli. Three
mitotic cells were found in 10 HPF. Thus, the histopathological diagnosis of second surgical specimen was papillary
meningioma, WHO Grade III. MIB-1 index was 19.4 %
(Fig. 2f). Two lesions again recurred after 23 months of
second surgery (Fig. 1h), which were surgically removed
and histologically revealed poorly differentiated tumor cells
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58
a
Brain Tumor Pathol (2015) 32:56–60
c
b
*
*
*
d
e
g
h
f
Fig. 2 Histopathology of initial and recurrent tumors. a Hematoxylin
and eosin (HE) staining revealed a patternless tumor tissue with
abundant intercellular collagen fiber and invasion of brain tissue
(9200). b HE staining revealed tumor cells with entrapped normal
brain parenchyma (asterisks) and right lower corner showing
immunohistochemistry of brain parenchyma positive for GFAP
(asterisk) (9100). c Tumor specimen showing strong immunostaining
for vimentin (9200). d MIB-1 staining of the tumor specimen
(9400). e HE staining of tumor tissue from the second surgery
showed discohesive growth with pseudopapillae and perivascular
pseudorosettes (9100). f MIB-1 staining of tumor specimen from the
second surgery (9400). g HE staining of third surgery specimen
revealed poorly differentiated tumor cells with brisk mitoses (arrows)
(9400). h MIB-1 staining of tumor specimen from the third surgery
(9400)
with mitotic count of more than 20 per 10 HPF (Fig. 2g).
Thus, the histopathological diagnosis of third surgical
specimen was anaplastic meningioma. MIB-1 index was
28 % (Fig. 2h). The third and tiny recurrence was detected
7 months after the last operation, which was under control
by stereotactic radiation using Gamma Knife with dose of
20 Gy. The patient is now, 57 months after the first surgery,
working as a clerical staff without any neurological deficit.
that only 1 % of those were intraventricular [6]. By Nakamura’s review, 78 % of IVMs were located in the lateral
ventricles, 16 % in the third ventricle, and 7 % in the
fourth ventricle [7]. To our knowledge, only eight papers
reporting third ventricular meningiomas have been previously published in the literature as shown in Table 1 [4, 5,
7–12].
Meningiomas are basically benign tumors and follow a
favorable clinical course. Most of the intraventricular
meningiomas are also low grade, but 5 out of 8 intra-third
ventricular meningiomas were reported to be of Grade II or
III [5, 7–9, 12] and one report did not mention the grade of
meningioma [11]. In our case, preoperative provisional
diagnosis was glioma arising from right thalamus. Intraoperative exploration confirmed large part of the tumor was
Discussion
Intraventricular meningiomas (IVMs) without dural
attachment are uncommon. In 1938, Harvey Cushing’s
personal series of 313 intracranial meningiomas showed
123
Strenger et al. [5]
Pandya et al. [11]
Huang et al. [9]
Nakamura et al. [7]
Bhatoe et al. [4]
Song et al. [12]
Wajima et al. [10]
Ødegaard et al. [8]
Present case
1.
2.
3.
4.
5.
6.
7.
8.
9.
49/M
NA
63/M
12/M
NA/F
25/M
6/M
10/M
61/F
Age
(year)/
sex
M male, F female, NA not available
Author
No
2.7 9 2.5 9 2.5 cm
NA
NA
2 cm
NA
7 cm
4 9 3 9 3 cm
NA
NA
NA
Size
Headache, left hemiparesis
Headache, vertigo, nausea,
vomiting
Headache
Headache, gait disturbance,
abnormal behavior, ataxia
Headache,
neurofibromatosis type 2
Mental change, motor
disturbance, visual deficit
Bifrontal headache,
vomiting, gait disturbance
Headache, vomiting, loss of
consciousness, bilateral
papilloedema
Confusion, gait ataxia, left
hemiparesis
Symptoms
Table 1 Reported cases of third ventricular meningioma with WHO grading
Transcorticaltransventricularsubchoroidal
Transcallosal
Right frontal transcorticaltransventricular
Left frontal transcorticaltransventricular
Transcorticaltransventricular
Transcallosal
NA
NA
Transventricular
Surgical
approach
Total
Total
Total
Total
Total
Subtotal
Debulking
Total
NA
Resection
NA
Atypical?
papillary ? malignant
Grade II ? III
Meningo-thelial
Chordoid
NA neurofibromatosis
NA
Atypical
NA, neurofibromatosis
NA
Histological subtype
Grade I and II
Grade I
Grade II
Grade I
Grade I and II
Grade II
NA
Grade III
WHO grading
Three times
recurrence
Good
Good
Good
Good
Death
(pneumonia)
Good
Good
Death
Outcome
Brain Tumor Pathol (2015) 32:56–60
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123
60
embedded in the thalamus. But the tumor had clear
attachment with third ventricular choroid plexus. So the
tumor was considered to have arisen from the choroid
plexus and extended into right thalamus due to the invasive
nature of the tumor.
In the present case, histology showed progression of
tumor into more malignant categories, from atypical
meningioma to papillary and anaplastic meningioma.
When meningiomas recur, progression to a higher histological grade is relatively uncommon but when this does
occur, the change is almost always by only one grade, even
with multiple recurrences like in present case [13]. In our
case, first surgery specimen comprised of meningothelial
atypical cells with increased cellularity, sheet-like growth,
small cells with a high N/C ratio, foci of necrosis; the
features being consistent with atypical meningioma (WHO
Grade II) [2]. The second surgery specimen showed discohesive growth with pseudopapillae, perivascular pseudorosettes in majority and mitotic cell count of 3 per 10
HPF, thus the diagnosis was papillary meningioma (WHO
Grade III) [1]. The third surgical specimen showed no
papillary pattern but more than 20 mitoses per 10 HPF
leading to the diagnosis of anaplastic meningioma (WHO
Grade III) [2]. MIB-1 also showed gradual increase of their
proliferative potential, from 8.3 to 19.4 % and then to
28.0 %. It has been reported that MIB-1 positive index is
very important for the biological and histopathological
analyses of meningiomas and for the prediction of recurrence and anaplastic transformation [14]. Reported series
have shown that 0.16–2 % of all meningiomas transform
into malignant variants [15] and that 14–28.5 % of recurrent benign meningiomas transform into atypical or anaplastic lesions [16]. Among atypical meningiomas,
26–33 % showed more anaplastic histologic features in
their recurrence [16]. It is reported that, the period of time
that elapsed to the anaplastic transformation ranged from
99.7 months (in women) to 177.75 months (in men) for
tumors first diagnosed as benign, and was considerably
shorter (40.8 months) for tumors first diagnosed as atypical
[17]. In our case the anaplastic progression was observed in
20 months. Follow-up MRI also showed further recurrences with short intervals. Considering quite high potential for anaplastic transformation of atypical meningioma,
close follow-up by enhanced MRI should be mandatory
even after the achievement of gross total resection.
In conclusion, third ventricular meningioma is rare,
difficult to diagnose and when present is mostly of high
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Brain Tumor Pathol (2015) 32:56–60
grade. Therefore, in case of third ventricular tumor
attached to the choroid plexus, it is preferable to consider
meningioma as a differential diagnosis. The probability of
its anaplastic transformation should also be taken into
account.
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