Key-words:
Falcine meningiomas - microsurgical resection - parasagittal meningiomas - radiosurgery
Introduction
As the second most common region of origin for intracranial meningiomas, the basic
pathological, anatomical, and surgical features of parasagittal and falcine meningiomas
are familiar to most neurosurgeons.[[1]],[[2]],[[3]],[[4]],[[5]],[[6]],[[7]] More specifically, the management of these tumors centers around the relationship
between the tumor and venous anatomy of the superior sagittal sinus (SSS), and the
large cerebral veins that enter the sinus in proximity of them.[[1]],[[5]],[[7]],[[8]],[[9]],[[10]] The propensity for these tumors to encase or adhere to cerebral veins, or to invade
the venous sinus, can greatly complicate our efforts to achieve the safe, complete
removal of the tumor and its involved dural base.[[1]],[[5]],[[7]],[[8]],[[9]],[[10]]
Over recent decades, stereotactic radiosurgery (SRS) and conformal radiotherapy (CRT)
have been established as safe and effective methods for limiting the growth of appropriately
sized meningiomas.[[7]],[[11]],[[12]] Some investigators have proposed the use of radiosurgery as the sole treatment
for most small parasagittal and falcine meningiomas, due to the lack of any markedly
radiosensitive structures in the vicinity of these tumors.[[7]],[[8]] In cases of small, minimally symptomatic tumors without imaging features that are
of concern or a known history of rapid growth on serial imaging studies, SRS or CRT
should be given serious consideration, even though we still consider surgery or a
“wait and see” strategy. In the last option, we perform magnetic resonance imaging
(MRI) contrast-enhanced examination every 6 months for the 1st year and then every
12 months.
In the present study, our aim was to address neurosurgical outcomes in a focused cohort
of patients with parasagittal and falcine meningiomas for which both SRS and transcranial
resection were considered for a state-of-the-art management. Our study series include
too patients from the era of radiosurgery in full, started in our Department in 1996,
whom outcomes data for neurosurgical treatment are most relevant for the present neurosurgical
practice.
Subjects and Methods
Patient population
These patients were adults (age ≥18 years) who underwent neurosurgical multidisciplinary
treatment at the authors' Neurosurgical Department between 1999 and 2013, had preoperative
MRI and postoperative computed tomography scan (CT-scan) imaging (<24 h), and had
at least 1 year of clinical and neuroradiological (MRI) follow-up. Patients with hemangiopericytomas
were excluded from the study. For each patient, MRI studies were reviewed to confirm
diagnosis of a parasagittal or falcine meningioma, which were defined as those that
primarily arose either from the falx or from the dura mater at the lateral edge of
the SSS. In general, surgical cases involved tumors >2.0 cm in largest diameter, tumors
with imaging features raising concerns for higher histological grade (that is, irregular
borders, an indistinct interface with the cortical surface), tumors growing rapidly
on serial imaging, and tumors with significant symptoms referable to mass effect.
Outcome assessment
Central pathological review was performed on the basis of the WHO guidelines.[[13]] Clinical data were collected from patient records and telephone interviews. All
clinical assessments were performed by a neurosurgeon. In each case, the extent of
resection and Simpson grade [[7]],[[14]],[[15]] were determined using a combination of the surgeon's assessment and MRI.
Neurosurgical strategy and perioperative management
Intraoperative neuronavigation was routinely used to minimize the skin incision and
craniotomy size while attempting a Simpson Grade 1 resection. Preoperative embolization
was not considered even for the large tumors because often, the vascular supply for
these larger tumors included pial supply. In general, en bloc resection was not attempted
for large tumors, due to tumor size, and instead the tumor was debulked from within
using an ultrasonic aspirator. Careful attention was paid to identifying and respecting
the arachnoid plane at the tumor–brain interface, which facilitates complete resection
and minimizes pial vessel injury. Whenever possible, involved dura was resected with
a 2-cm circumferential margin, and the dura was closed with either a pericranial graft
or the artificial dura substitute. For lesions with bone invasion, the craniectomy
site was repaired using methyl methacrylate. For larger cranial defects, a preoperative
custom-made cranioplasty was used.
Although the goal of the operation from the outset was total tumor removal, the discovery
of significant involvement of the SSS or the bridging cortical veins often limited
these attempts and was managed as follows. We generally do not resect patent cortical
bridging veins involved with tumor, and we leave tumor remnants that are densely adherent
to these vessels. Completely occluded venous sinuses were resected, taking care to
spare any patent cortical bridging veins on the edges of the occluded portion of the
sinus. Complete sinus occlusion was generally confirmed using the venous phases obtained
during the digital subtraction angiography (DSA) studies or a technically adequate
MR venogram as evidence of complete sinus occlusion. More commonly, we noted invasion
of tumor into a patent sinus. In case of small invasion of the SSS, tumor can be removed
using patient microsurgical dissection of the dura layers, with hemostasis obtained
with bipolar coagulation, or hemostatic agents combined with fibrin glues or reconstructions
techniques when necessary. We do not attempt removal of larger degrees of tumor invasion
of a patent sinus and instead leave this portion of the tumor, which is observed using
serial imaging, and treated with radiosurgery immediately postoperatively, or the
time of progression or with surgery if the sinus is completely occluded by the tumor.
For falcine meningiomas, that portion of the falx below the SSS is resected after
the bulky tumor is removed. This then qualifies the removal as Simpson Grade 1.
Intraoperatively, all patients received Decadron (8 mg), mannitol (1 g/kg), and ceftriaxone
(2 gr) at the time of incision. On postoperative day 1, a prophylactic dose of enoxaparin
(4000 UI subcutaneously each day) was initiated in all patients and continued for
2 weeks. Routine use of venous thrombosis prophylaxis was not started until after
1999.[[7]],[[16]] The incidence of postoperative intracranial hemorrhage was no different in the
patient groups before or after prophylaxis was begun.[[7]],[[17]] Irrespective of preoperative seizure history, all patients had also received loading
doses of an antiepileptic agent at the time of surgery (Dintoin initially, Keppra
most recently), which was continued for 2 weeks postoperatively and then discontinued.
In the immediate postoperative period (<24 h), a CT-scan imaging was performed to
all patients. MRI was performed at 6-month intervals for all patients for a period
of 2 years. For those patients with known residual tumor after surgery, and those
with WHO Grade II or III tumors, MRI was continued at 1-year interval. Patients with
gross totally resected WHO Grade I tumors were followed clinically and with MRI at
2-year interval. In case of new or worsened symptoms, urgent MRI was performed. Recurrence
was defined as any unequivocal, new enhancement in the resection cavity. Tumor progression
was defined as any unequivocal increase in the size of the residual tumor seen on
the immediate postoperative imaging. For purposes of comparing rates of tumor control,
recurrence and progression were treated as a similar event.
Statistical analysis
Statistical analysis was performed using the Kaplan–Meier method. Binary variables
were compared using the Pearson Chi-square test. Continuous variables were compared
using an independent samples t-test or ANOVA, after statistical confirmation of data
normality. Continuous variables are presented as the mean ± standard error. Statistical
tests were considered significant when P < 0.05 after correcting for multiple comparisons
using the Bonferroni method. All odds ratios reflect the risk of having new or worse
neurological dysfunction after surgery.
Results
Demographics and presenting symptoms
We identified 100 patients with symptomatic, and/or growing, >2.0 cm in the largest
diameter parasagittal/falcine meningiomas who underwent multidisciplinary neurosurgical
treatment of their lesion at our department between 1999 and 2013. The median length
of follow-up was 6.9 years (range 1–15 years). The basic demographics are summarized
in [[Table 1]]. Significant invasion of SSS was noted in 46 (46%) of 100 cases. The age and sex
distribution of these patients did not differ significantly from that in patients
without sinus invasion. Tumors invading the sinus were more commonly WHO Grade II
or III (58% vs. 32%, P < 0.01), commonly larger, but there was no difference in histopathological
type between tumors associated with the anterior, middle and posterior thirds of the
sinus. There was no WHO Grade III meningiomas in patients referred to the group without
sinus invasion.
Table 1: Demographic data in 100 patients with parasagittal/falcine meningiomas
The presenting symptoms for patients in this series are summarized in [[Table 2]]. Approximately one-third of all patients, many of whom had tumors more than 4 cm
in largest diameter, presented without referable symptoms or deficits (35 of 100).
Headaches (in 25 of 100) and seizures (in 16 of 100) occurred commonly. Ataxia/gait
disturbance, unilateral weakness occurred as frequently as lower extremity weakness.
Notable was the interesting occurrence of new-onset psychotic symptoms in 5 patients,
3 of whom demonstrated invasion of the SSS.
Table 2: Presenting symptoms in patients in this series
Management of superior sagittal sinus invasion and the impact on tumor control
Four of 46 patients with sinus occlusion were found to have complete sinus occlusion
on preoperative studies, and the involved portion of the sinus was fully resected
in all 4 patients. None of these patients experienced recurrence of their tumor over
a median follow-up period of 9.9 years (range 2.6–13.4 years). In 30 of 42 cases,
the sinus invasion was minor and could be removed using careful microsurgical dissection,
with hemostasis obtained using gel foam, fibrin glue, and occasionally suturing the
sinus wall. In the other 12 cases, more significantly sinus invasion was noted, and
the tumor was subtotally resected, the exposed attachments coagulated, and the remnant
tumor left in the sinus. Nine of the 12 patients undergoing subtotal resection (STR)
received SRS within 3–5 months after surgery to treat the residual tumor in the sinus
(60 Gy in 20 fractions). One (WHO Grade III) of the patients who received upfront
radiosurgery, demonstrated subsequent tumor growth during follow-up (5.2 years postoperatively),
and was treated with repeat surgery. None of the other seven patients who received
upfront radiosurgery demonstrated any evidence of subsequent tumor growth over a follow-up
period of 9.3 years (range 2.1–14 years). One of the 30 patients receiving complete
tumoral removal and one of the three receiving STR experienced tumor recurrence or
progression over a follow-up period of 7.7 years (range 1.7–15 years). All 2 patients
with recurrence had WHO Grade II tumors, which were treated with repeat surgery at
the time of recurrence. Of the 54 patients in which no sinus invasion was found at
surgery, gross total resection (GTR) was obtained in 51 of them. In the cases in which
STR was performed, the tumor was adherent to bridging veins, which forced an STR to
spare venous anatomy. All 3 patients undergoing STR, underwent radiosurgery within
3 months of surgery (60 Gy in 20 fractions). For all of them (WHO Grade II tumors)
there was no evidence of subsequent tumor recurrence or progression during follow-up.
There were 2 recurrences in the patients who underwent GTR, involving WHO Grade II
tumors, which recurred at 3.45 and 5.75 years postoperatively, and were treated with
repeat surgery at the time of recurrence. In this series, there were no patients who
had WHO Grade I GTR, which recurred at the overall period of follow-up.
We performed Kaplan–Meier analysis for patients with WHO Grade I tumors to compare
recurrence/progression-free survival for patients GTR versus STR. Patients who underwent
upfront radiosurgery to the remnant lesion following STR were excluded from this analysis,
to study the natural history of small tumor remnants that remained in the SSS or were
attached to the veins. As seen in [[Figure 1]], there was no difference in rates of tumor control for patients who received STR
for a Grade I tumor, followed by close observation, compared with those undergoing
GTR, primarily because we did not observe any cases in which the tumor remnant in
the SSS demonstrated interval growth on serial imaging studies.
Figure 1: Kaplan-Meier survival plot for patients with a WHO Grade I tumor who were not treated
with early postoperative radiosurgery, comparing recurrence/progression-free survival
for patients who underwent gross total resection versus intentional subtotal resection
in which tumor was left in the superior sagittal sinus or attached to bridging cortical
veins. NS - Not significant
Morbidity
In this series, 87% of patients did not experience any complications as a result of
neurosurgical treatment [[Table 3]]. Three of 100 patients experienced new or worsened neurological deficits after
surgery, referable to surgical manipulation around the motor strip. Medical complications
were relatively uncommon (5 of 100 patients). Neurosurgical/radiosurgical complications
constituted the majority of complications in this series (8 of 100 patients). Brain
edema was the most common complication (including 2 patients underwent SRS for residual
tumor within 3 months of surgery). None of the four patients with brain edema required
surgical treatment. There was 1 episode of venous infarction noted. The cause of venous
infarction in this case was not determined; however, it did not occur in a patient
with a known vein sacrifice, or with documented venous sinus thrombosis.
Table 3: Medical and neurosurgical morbidity in 100 patients with parasagittal/falcine meningiomas
Discussion
In this study, we reported our experience with neurosurgical management of parasagittal
and falcine meningiomas in a focus of patients, who author believes best represent
the volume of patients treated in contemporary neurosurgery, namely those with meningiomas
>2.0 cm in the largest diameter. These tumors are frequently symptomatic, often higher
grade, and in some cases are massive. More than one-third of the tumors in this series
exceeded 4 cm in diameter, and 7 tumors in this series exceeded 8 cm in diameter.
Despite these challenges, we have found that complete resection or good tumor control
with acceptable low rates of morbidity can be achieved with advanced microneurosurgical
techniques and thoughtful consideration of the venous anatomy and its relationship
to the tumor.
A principal goal of our analysis was to provide data in addition to the outcomes for
patients with these tumors, regarding the surgical and clinical significance of invasion
of the SSS. Whereas tumors causing complete sinus occlusion can usually be removed
in their entirety, and tumors that do not invade the sinus can usually be resected
without great difficulty, the management of tumors invading the SSS and causing incomplete
sinus occlusion has always posed the greatest surgical dilemma.[[1]],[[2]],[[3]],[[18]] The continuous evolution of microneurosurgical techniques led to an increasingly
aggressive attempts at complete surgical removal of parasagittal meningiomas.[[5]],[[9]],[[19]],[[20]],[[21]] In this treatment paradigm, complete resection is the goal of all surgeries, with
direct surgical removal of tumor from the sinus performed if necessary. Maintenance
of central venous outflow in this approach is achieved using surgical patching of
the sinus, or a bypass procedure if necessary.
This study presents our results with the alternate approach of removing as much tumor
as possible while preserving major cortical veins and leaving tumor remnants that
significantly involve the sinus.[[7]],[[8]]
In this approach, as previously reported by Sughrue et al.,[[7]] the residual tumor can be followed closely with serial imaging and treated with
radiosurgery or repeat surgery in the event of subsequent growth. We have found that
even with minor degrees of sinus invasion, we were able to remove all of the tumor
without heroic efforts. The tumor control rates we have observed are excellent, with
the majority of the recurrences that we observed resulting from higher grade tumor
histopathological features. These data suggest that small residual portions of WHO
Grade I tumors left in and around the SSS do not grow appreciably for several years
after surgery, even without adjuvant radiation-based treatments.
The results do not obviate the need for many years of close imaging follow-up, but
they suggest that radiosurgical management of residual disease might be delayed or
even avoided in some patients. We support that in general these data suggest a move
toward less aggressive resection in cases of tumor invasion of a patent sinus. In
cases of minor invasion, we will continue to attempt to address these fragments surgically.
However, given our good results by simply leaving tumor in the sinus, following the
remnant with serial imaging, and managing recurrences with radiosurgery or repeat
surgery, it seems less necessary to be surgically heroic in these cases.
In cases involving the anterior one-third of the SSS in which the MR venogram or four
vessel DSA shows at least 2 other draining veins on the opposite side, remote from
the region of involved sinus, we believe it is safe to consider limited or even complete
sinus resection. In cases of complete occlusion of the SSS, total excision is safe.
However, in cases with incomplete occlusion, or when there are fewer than 2 veins
on the opposite side, separation of the leaves of the dura matter preserving the inner
layer of the lateral wall of the SSS is acceptable.
Close observation and radiosurgery as needed are important in the management of WHO
Grade I tumors that invade a patent sinus, especially for remnants in the middle and
posterior one-third of the sinus. The data of our study suggest that in many cases,
radiosurgery can be delayed because many tumor remnants in the sinus do not grow on
serial imaging. Planning resection and grafting of the sinus, given the great rates
of tumor control seen in radiosurgery, seems of no role in the neurosurgical management
of these tumors. As previously reported by Smith et al.,[[22]] we treat WHO Grade II tumors with selective use of radiotherapy. We treat all WHO
Grade III tumors with external beam radiotherapy.[[23]]
Conclusions
Authors present their experience with neurosurgical management of parasagittal/falcine
meningiomas >2.0 cm in the largest diameter. The fact the median follow-up period
is of 9.9 years in our analysis can be considered as a limitation of our study. However,
these data provide a judicious modern estimate of the expected outcomes that can be
obtained after treating patients with these tumors, using a combination of advanced
microneurosurgical techniques and tools, image guidance, and treatment with CRT.
