Keywords
high-grade meningioma - recurrent chronic subdural hematoma - outer membrane of subdural
hematoma
The incidence of recurrent chronic subdural hematoma (CSDH) accounts for ∼5 to 33%
of postsurgical cases.[1] CSDH recurs most frequently between 1 and 3 months after surgery.[1] Early recurrence of CSDH is determined as relapse of symptoms or re-accumulation
of the hematoma within 3 months following surgery.[1] There are many etiologies for recurrence of CSDH.[1]
[2] Subdural hematoma is a less frequent complication in meningioma.[3] Besides, CSDH is rarely associated with meningioma.[3] [Table 1] summarizes previously reported cases of meningioma in association with CSDH.[3]
[4]
[5]
[6]
[7]
[8]
[9]
[10]
[11]
[12]
[13]
[14]
[15]
[16]
[17]
[18] Although several mechanisms to cause subdural hematoma in meningioma have been previously
reported,[3]
[15]
[19] our case suggested a different mechanism from them. We describe a case of malignant
subdural hematoma that rapidly and repeatedly recurred in association with meningioma.
Table 1
Summary of previously reported cases of meningioma associated with chronic subdural
hematoma
|
|
|
|
|
CSDH
|
Meningioma
|
|
|
No.
|
Author
|
Year
|
Sex
|
Age
|
Side
|
Side
|
Location
|
Histology
|
Outcome
|
|
1
|
Cusick and Bailey[4]
|
1972
|
F
|
47
|
Bilateral
|
Right
|
Convexity
|
Transitional
|
Dead
|
|
2
|
Modesti et al[5]
|
1976
|
F
|
49
|
Left
|
Left
|
Parasagittal
|
Meningothelial
|
SD
|
|
|
|
M
|
69
|
Left
|
Left
|
Convexity
|
Meningothelial
|
GR
|
|
3
|
Walsh et al[6]
|
1977
|
F
|
77
|
Right
|
Right
|
Olfactory groove
|
Meningothelial
|
Dead
|
|
4
|
Sakai et al[7]
|
1981
|
M
|
36
|
Right
|
Right
|
Sphenoid ridge
|
Meningothelial
|
Dead
|
|
5
|
Baskinis et al[8]
|
1984
|
M
|
68
|
Right
|
Right
|
Convexity
|
Angiomatous
|
GR
|
|
6
|
Tomita et al[9]
|
1985
|
F
|
61
|
Right
|
Right
|
Convexity
|
Meningothelial
|
GR
|
|
7
|
Wang et al[10]
|
1985
|
F
|
62
|
Left
|
Left
|
Convexity
|
N/A
|
N/A
|
|
8
|
Itoyama et al[11]
|
1987
|
F
|
63
|
Bilateral
|
Left
|
Sphenoid ridge
|
Transitional
|
GR
|
|
9
|
Chen et al[12]
|
1992
|
M
|
79
|
Left
|
Left
|
Convexity
|
Meningothelial
|
MD
|
|
10
|
Pozzi et al[13]
|
1993
|
F
|
73
|
Left
|
Left
|
Convexity
|
Transitional
|
N/A
|
|
|
|
F
|
85
|
Left
|
Left
|
Convexity
|
N/A
|
N/A
|
|
11
|
Popovic et al[14]
|
1994
|
F
|
47
|
Right
|
Right
|
Convexity
|
Meningothelial
|
N/A
|
|
12
|
Tanaka et al[15]
|
1994
|
F
|
47
|
Right
|
Right
|
Convexity
|
Meningothelial
|
GR
|
|
13
|
Sinha and Dharker[16]
|
2001
|
M
|
68
|
Left
|
Right
|
Convexity
|
N/A
|
GR
|
|
|
|
F
|
70
|
Left
|
Right
|
Convexity
|
N/A
|
GR
|
|
14
|
Di Rocco et al[3]
|
2006
|
M
|
72
|
Right
|
Right
|
Convexity
|
Meningothelial
|
GR
|
|
|
|
M
|
74
|
Left
|
Left
|
Convexity
|
Transitional
|
GR
|
|
15
|
Czyz et al[17]
|
2011
|
F
|
69
|
Bilateral
|
Bilateral
|
Parasagittal
|
N/A
|
GR
|
|
16
|
Nery et al[18]
|
2017
|
F
|
85
|
Left
|
Left
|
Convexity
|
Microcystic
|
GR
|
Abbreviations: CSDH, chronic subdural hematoma; GR, good recovery; MD, moderate disability;
N/A, not applicable; SD, severe disability.
Case Report
A 70-year-old man, who had previously undergone surgical resection of left parasagittal
meningioma involving the middle third of the superior sagittal sinus (SSS) two times,
presented with right lower limb weakness. The first and second removals of the tumor
via open surgery remained as Simpson grade IV because of hardening of the tumor and
adhesion to surrounding structures including the SSS. The remaining tumor massively
recurred within 1 year after the last discharge despite γ-knife radiosurgery following
the second tumor removal ([Fig. 1a–c]). We attempted removal of the tumor combined with SSS resection because obstruction
of the SSS caused by the developed tumor was confirmed. The tumor was consequently
removed as Simpson grade II. The residual tumor, including the dural tail sign, was
not observed on postoperative magnetic resonance imaging ([Fig. 1d–f]). The third histopathological result showed an atypical meningioma, World Health
Organization (WHO) grade II. Postoperatively the patient was transferred to a rehabilitation
hospital.
Fig. 1 (a–c) Preoperative MRI showing recurrent left parasagittal meningioma located in the middle
third of the superior sagittal sinus. (d–f) Postoperative MRI showing tumor removal combined with superior sagittal sinus resection
as Simpson grade II without distinct dural tail sign. MRI, magnetic resonance imaging.
The patient who manifested a progressive headache was readmitted with a diagnosis
of left dominant bilateral CSDH 1 month after removal of the tumor ([Fig. 2a]). He had no clinical history, such as head injury, antithrombotic therapy, coagulation
disorders, and alcohol abuse. In addition, postoperative images revealed no signs
of CSDH. The left subdural hematoma alone was treated by burr hole surgery, which
was successful ([Fig. 2b]). However, recurrence of CSDH occurred 5 days after surgery. Although a second burr
hole evacuation of subdural hematoma was performed, a third evacuation was required
owing to its rapid recurrence within 2 days after the second evacuation. Because CSDH
eventually changed to acute subdural hematoma ([Fig. 2c]), craniotomy was accomplished 10 days after the third hematoma evacuation ([Fig. 2d]). The hematoma and outer membrane of the subdural hematoma were eliminated as much
as possible. Furthermore, the dura mater within the craniotomy area was removed and
replaced with artificial dura mater. Histopathological features of the outer membrane
of the subdural hematoma showed anaplastic meningioma, WHO grade III. Unfortunately,
the patient died of worsening of general condition despite aggressive treatment one
and a half months since the onset of CSDH although the subdural hematoma had obviously
not recurred. His brain was investigated by autopsy after death. Histopathology of
brain autopsy demonstrated invasion of anaplastic meningioma cells spreading to the
whole outer membrane of the subdural hematoma ([Fig. 3]).
Fig. 2 (a) CT on the readmission showing left dominant bilateral CSDH appeared after tumor
removal. (b) Postoperative CT of the first burr hole surgery showing resolution of CSDH. (c) Preoperative CT of hematoma elimination with craniotomy showing left acute subdural
hematoma changed from repeatedly recurrent CSDH. (d) Postoperative CT of craniotomy showing elimination of acute subdural hematoma. CSDH,
chronic subdural hematoma; CT, computed tomography.
Fig. 3 Histopathological photomicrograph of the brain autopsy. (a) H&E stain and (b) epithelial membrane antigen immunostain of coronal brain section showing the outer
membrane of the subdural hematoma entirely infiltrated by meningioma cells. Magnification,
×10. (c) High-magnification image of the black dotted square box of the H&E stain revealing
high cellular density, nuclear polymorphisms, and numerous mitoses, indicating anaplastic
meningioma. Magnification, ×400. H&E, hematoxylin and eosin; SSS, superior sagittal
sinus.
Discussion
Numerous causative factors for recurrence of CSDH have been addressed including advanced
age, antithrombotic medications, coagulopathy, and various neuroimaging features of
hematoma.[1]
[2] Although subdural hematoma formation in meningioma is rare, several mechanisms have
been proposed as follows[3]
[15]
[19]: (1) bleeding of the tumor into the subdural space, (2) rupture of abnormal vascular
networks supplying the tumor in the subdural space, and (3) collapse of the subdural
vessels due to compression of the tumor.
No correlation between the occurrence of subdural hematoma and the location or histological
characteristics of meningioma has been described.[15]
[20] On the other hand, the malignant histological type has been reported with a high
frequency in meningioma complicated with subdural hematoma.[15]
[20] Patil observed that a dural reaction of the meningioma formed the neomembrane similar
to the outer membrane of CSDH despite neither subdural fluid collection nor blood
clots.[21] Moreover, they noticed that tumor cells were not expressed in the neomembrane originating
from the meningioma.[21] In our case, the outer membrane of the subdural hematoma was entirely infiltrated
by meningioma cells. To the best of our knowledge, no previous report has mentioned
similar findings to our case. Meningioma with malignant transformation is indicated
to acquire hematogenous spread.[22] The outer membrane of CSDH is highly vascularized and enriched with numerous capillaries.[1] Invasion of meningioma cells might occur hematogenously to the outer membrane of
CSDH. Otherwise, meningioma in our case might have had capsule-like growth along the
dura as en plaque meningioma. Formation of subdural hematoma related to a malignant
tumor is considered to be the result of capillary dilatation and rupture of the outer
membrane via fine vessel obstruction by tumor cells.[23] In high-grade meningioma, vascular endothelial growth factor (VEGF) is expressed
and involved in permeabilization of blood vessels as well as tumor angiogenesis and
vasculogenesis.[24] VEGF is detected in the outer membrane of CSDH and has an association with expansion
of hematoma and recurrent bleeding.[25] Therefore, disruption of vulnerable tumor vessels or the effect of VEGF may allow
the outer membrane infiltrated by meningioma cells to exude the hematoma into the
subdural space.
An effective treatment strategy for subdural hematoma associated with meningioma is
the elimination of hematoma at the same time as removal of the tumor.[19]
[26] Early surgical intervention is advocated, especially in cases accompanying acute
subdural hematoma.[20] Our case had rapid and repeated recurrence of subdural hematoma despite prompt evacuation
of the hematoma, eventually leading to death. Removal of the outer membrane surrounding
subdural hematoma is presently not regarded as important.[1] However, the prognosis of our patient might have been improved by early removal
of not only the hematoma but also as much of the outer membrane as possible.
In the case of CSDH associated with meningioma, especially high-grade meningioma,
histopathological features of the outer membrane of subdural hematoma should be investigated.
The subdural hematoma needs to be treated with caution when tumor infiltration is
demonstrated in the outer membrane.
