Abstract
Objective
Tentorial meningiomas are complex lesions that may not always be completely resected without significant morbidity or mortality. In this study, we evaluate the outcomes of tentorial meningiomas treated with Gamma Knife radiosurgery (GKRS).
Methods
We performed a retrospective review of a prospectively compiled database evaluating the outcomes of 35 patients with tentorial meningiomas treated at the University of Virginia from 1990 to 2006. There were 29 females and 6 males with a median age of 60 years (range 21-82). Twenty were treated with primary radiosurgery, and 15 patients were treated with adjuvant radiosurgery after surgical resection. Patients were assessed clinically and radiologically at routine intervals following GKRS. Kaplan-Meier analysis was used to assess tumor progression.
Results
The mean follow-up was 5 years (range 2-16 years). The mean pre-radiosurgery tumor volume was 5.1 cc (range 0.7-27.3cc). At last follow-up, 31 patients (89%) displayed either no growth or a decrease in tumor volume. Four (11%) patients displayed an increase in volume. Kaplan Meier analysis demonstrated radiographic progression free survival at 3, 5, and 10 years to be 96%, 91%, and 73% respectively. At the last clinical follow-up, 33 patients (94%) demonstrated no change or improvement in their neurological condition and 2 patients clinically declined (6%).
Conclusion
GKRS offers an acceptable rate of tumor control for tentorial meningiomas, and accomplishes this with a low incidence of new or worsening neurological deficits.
Keywords: Radiosurgery, gamma knife, meningioma, tentorium
INTRODUCTION
Meningiomas represent one of the most common intracranial tumors in adults. The majority of meningiomas are histologically benign and classified as WHO grade I. For those that are atypical or malignant meningiomas (i.e. WHO grade II and III), they exhibit a substantially more aggressive behavior. The behavior of atypical and malignant meningiomas is characterized by brain invasion and a high likelihood of recurrence. All treatment options including microsurgery, radiation therapy, and radiosurgery demonstrate less effectiveness for patients with atypical and malignant meningiomas.
WHO grade I meningiomas are extra-axial lesions and tend to displace rather than invade brain. They may, however, encase critical cerebrovascular structures such as cranial nerves or venous structures. Meningiomas typically demonstrate uniform contrast enhancement on imaging studies (i.e. magnetic resonance [MR] or computed tomography [CT]) with a distinct margin. The attributes make most WHO grade I meningiomas amenable to stereotactic radiosurgery.
Over the past two decades, stereotactic radiosurgery has come to occupy an increasingly important role in the treatment armamentarium for meningiomas. Radiosurgery’s potency and precise dose delivery to the target usually leads to long-term tumor control. The steepness of dose fall-off typically affords neurological preservation of surrounding critical structures. While microsurgical resection remains the primary treatment modality for many of these tumors, radiosurgery has become an important adjuvant treatment, and in some cases a primary treatment.
Meningiomas of certain locations present particular challenges with regard to radiosurgical management. Tentorial based meningiomas which comprise 2-7% of intracranial meningiomas are particularly complex as they can span both the supratentorial and infratentorial compartments (1, 3-5). They can frequently exert mass effect on the brainstem or cerebellum leading to neurological signs or symptoms. They can also abut the cerebral aqueduct causing hydrocephalus. The tumors may be in close proximity to or even encase deep draining veins or large sinuses.
For asymptomatic patients, radiosurgery has been used to treat small to moderately sized tentorial meningiomas that have been radiologically identified and diagnosed as likely benign, grade I neoplasms. Tentorial meningiomas with mass effect causing symptoms can generally be relieved through a resection; this also has the benefit of providing a firm histologic diagnosis. However, because of the neuroanatomical challenges of a gross total (i.e. Simpson grade I) resection of meningiomas in this area and the favorable benefit to risk profile of stereotactic radiosurgery, a maximal, safe resection followed by radiosurgery has become a common combined approach.
In this paper, we review our institutional experience using stereotactic radiosurgery for tentorial based, WHO grade I meningiomas. We evaluate the risks and benefits of Gamma Knife radiosurgery for patients with tentorial based meningiomas.
MATERIALS AND METHODS
Patient Population
This is a retrospective analysis of a prospectively maintained, IRB approved database. From 1989 to 2006, 752 patients with intracranial meningiomas were treated with GKRS at the University of Virginia. The diagnosis was confirmed either by tissue pathology or characteristic findings for meningiomas on neuroimaging studies.(2) Exclusion criteria included patients with multiple meningiomas, follow-up less than 24 months, or a confirmed tumor histological grade greater than WHO grade I. Consequently, 35 patients with tentorial meningiomas qualified for this study and were included in the analysis.
Patients were considered for radiosurgery if the meningioma was less than 35mm in diameter and if the patient was not disabled by their tumor (i.e. Karnofsky Performance Status of less than 70). Patients were not candidates for primary surgical treatment based on their advanced age, the projected operative risks based on medical comorbidities, and/or refusal of microsurgical resection. Adjuvant radiosurgical treatment was carried out in patients with recurrence or re-growth of lesions following microsurgical excision or as part of multimodality treatment wherein the risks of complete surgical resection outweighed the benefits of multimodality therapy.
Radiosurgical Technique
Patients underwent placement of a stereotactic Leksell G-frame in the operating room. During frame placement, they received monitored anesthesia administered by an anesthesiologist. Stereotactic magnetic resonance (MR) imaging was then obtained for the treatment planning. Pre and post-contrast thin slice (1 mm) axial and coronal MR sequences were obtained. When an MR imaging was not able to be obtained because of medical reasons (e.g. a cardiac pacemaker), a thin slice stereotactic CT was obtained with and without contrast. Radiosurgical dose plans were formulated under direction of a neurosurgeon in conjunction with a medical physicist and radiation oncologist.(7) The Leksell Gamma Unit Model U was used until July 2001 when the C model (Elekta Instruments, Inc., Norcross GA) was instituted. The Kula software was used for dose planning from 1989 to June 1994, and then subsequently Elekta’s Gamma Plan software (Norcross, GA) was used.
Follow up
Patients were typically followed clinically and radiologically every six months for the first year, annually until year five after radiosurgery, and then every two years thereafter. At each follow up visit, a neurological examination was performed to evaluate for new neurological deficits, and neuro-imaging studies were reviewed to assess tumor response. All follow-up was performed at the University of Virginia, unless the patient was unable to travel to our institution. In such cases, the referring physician performed the follow-up and provided documentation of the patient’s neurological status as well as follow-up imaging. Information from the referring physician was reviewed by the Gamma Knife team and appropriate recommendations were made.
Both a neurosurgeon and neuroradiologist at the University of Virginia reviewed all neuro-imaging studies. Imaging outcome was determined by the last available exam.(6) A decrease or increase in tumor size was defined as a 15% or greater change in tumor volume as compared to the volume at the time of GKRS.(6) In order to make this determination of tumor size, the tumor was outlined on radiographic images and serial volumetric calculations were performed using Image J in all patient imaging studies (NIH, Bethesda, MD). (6) Kaplan-Meier assessment of tumor progression was calculated.
RESULTS
Of the 35 patients with tentorial meningiomas, there were 29 females and 6 males with a median age of 60 years (range 21-82) at the time of radiosurgery. The most common symptoms or signs on presentation were headache (n=20; 57%), dizziness (n=13; 37%), CN VII dysfunction (n=7; 20%), ataxia (n=3; 9%), change in body sensation (n=2; 6%), and body weakness (n=4; 11%). Twenty patients who displayed neuro-imaging and clinical features consistent with benign meningiomas were treated with upfront radiosurgery. Fifteen patients were treated following surgical resection of a histologically confirmed WHO grade I meningiomas. Pre-operative patient and tumor characteristics are presented in Table 1.
Table 1.
Pre-operative patient and tumor characteristics
| Female:male | 29:6 |
| Mean age in years (range) | 60 (21-82) |
| Presenting signs/symptoms (n, %) | |
| Headache | 20 |
| Dizziness | 13 |
| CN VII dysfunction | 7 |
| Weakness | 4 |
| Ataxia | 3 |
| Change sensation | 2 |
| Number of prior surgery(ies) (n) | |
| None | 20 |
| Once | 13 |
| Twice | 2 |
GKRS, Gamma Knife radiosurgery; n, number of patients
GKRS planning was carried out with MRI in 29 cases (85%) and CT scan in 6 cases (15%). The mean maximum dose to the tumor was 35 Gy (range 20-60), the mean tumor margin dose was 15 Gy (range 10-20), and the mean prescription isodose line was 43% (range 30-55). The median number of isocenters used was 4 (range 2-19). Radiosurgical parameters are detailed in Table 2.
Table 2.
Radiosurgical parameters
The mean follow-up was 5 years (range 2-16 years). The mean pre-radiosurgery tumor volume was 5.2 cc (range 0.66-27.3cc) versus post-radiosurgery tumor volume of 3.2 cc (range 0-14.1cc). At the last follow-up, 31 patients (89%) displayed no change or decrease in tumor volume, 4 (11%) displayed an increase in volume. Overall patient outcomes are demonstrated in Table 3. Kaplan Meier analysis demonstrated radiographic progression free survival at 3, 5, and 10 years to be 96%, 91%, and 73% respectively (Figure 1).
Table 3.
Patient outcomes at last follow-up
Figure 1.
Kaplan-Meier progression free tumor survival
At the last clinical follow-up, 33 patients (94%) demonstrated no change or improvement in their neurological condition, and 2 patients clinically declined (6%). On follow-up imaging, 2 patients (5.7%) displayed new evidence of peritumoral edema. Following GKRS, 2 patients (5.7%) required surgical resection, and 1 patient (2.9%) required ventriculoperitoneal shunting for hydrocephalus.
Case 1 Example
A 64 year old female initially presented with headaches, imbalance, frequent falls, slurred speech, and short-term memory deficits. MRI identified a meningioma arising from the right tentorial leaflet and projecting inferomedially onto the underlying right cerebellar vermis. She refused surgical resection and, as such, was offered GKRS.
MRI obtained at the time of GKRS demonstrated a meningioma measuring 1.8 ml in volume (Figure 2). A dose plan was developed utilizing eleven isocenters; the tumor received 15 Gy to the 50% isodose line and a maximum dose of 30 Gy. Follow-up imaging 81 months after radiosurgery revealed that the tumor had decreased to 0.8 cc in volume, demonstrating a 55.6% decrease. During the years after her treatment, the patient had no progression of her symptoms.
Figure 2.
Case 1 Example
Top panel: T1-weighted, contrast-enhanced MR images taken prior to GKRS treatment demonstrating a meningioma (1.8 cc) arising from the medial aspect of the right tentorial leaflet and extending inferomedially onto the underlying right cerebellar vermis.
Bottom panel: MR images taken 81 months after treatment demonstrating a 55.6% decrease in tumor volume (0.8 cc).
Case 2 Example
A 51 year old female had a six month history of headaches, nausea, and vomiting. A left tentorial meningioma was indentified on MRI, and she underwent a left posterior fossa craniotomy and total resection of the tumor. After her surgery, she denied any headache, nausea, vomiting, seizures, visual changes, gait difficulty, or other neurologic deficits. A 2 mm recurrence was found on follow-up MRI 40 months after her surgery. Further follow-up imaging one year later showed that the recurrent tumor had grown to 12 mm maximum thickness, and she was referred to our institution for GKRS. She remained symptom-free at the time of her referral.
An MRI obtained at the time of GKRS indentified a meningioma measuring 20.33mm in maximum dimension and arising from the lateral aspect of the left tentorium immediately adjacent to the transverse sinus [Figure 3]. The tumor received a peripheral dose of 9.9 Gy to the 30% isodose line and a maximum dose of 33 Gy. Follow-up imaging 86 months after treatment revealed that the tumor had demonstrated a 51% decrease in size. The patient has required no further treatment for her meningioma and continues to be without symptoms.
Figure 3.
Case 2 Example
Top panel: T1-weighted, contrast-enhanced MR images taken for GKRS treatment planning demonstrating a meningioma (20.33 cc) arising from the lateral aspect of the left tentorium immediately adjacent to the transverse sinus.
Bottom panle: MR images taken 86 months after treatment demonstrating a 51% decrease in tumor volume (10 cc).
Case 3 Example
A 66 year old female initially presented with a five year history of transient intermittent diplopia, bilaterally tinnitus, and headaches. She was previously diagnosed with recurrent migraine headaches. When her symptoms began, an MRI was obtained and was reportedly normal. She had also had full ophthalmologic evaluation and otolaryngology evaluation, which were both unremarkable. She tolerated her symptoms for about five years at which time her bouts of diplopia and bilateral tinnitus increased in frequency. She expressed that her symptoms varied with changes in position of her head and closing her eyes. Another MRI was obtained and demonstrated a left tentorial tumor. At that time, it was noted that there was no clear connection between the lesion seen on neuroimaging and her symptomatology, so her neurosurgeon recommended against surgery and referred her for GKRS.
An MRI obtained at the time of GKRS demonstrated a tumor arising from the left tentorial edge with compression of the pons consistent with a meningioma [Figure 4]. The lesion measured 1.7 cc in volume at the time of treatment. The tumor received a peripheral dose of 15 Gy to the 50% isodose line and a maximum dose of 30 Gy. Follow-up MRI obtained 41 months after her treatment showed that the tumor had decreased to 0.8 cc in volume, demonstrating a 53% decrease in size. Despite this shrinkage, the patient experienced no improvement or deterioration of her symptoms after her GKRS treatment. Her clinical status remained stable up until 39 months when she had an unrelated cerebrovascular accident.
Figure 4.
Case 4 Example
Top panel: T1-weighted, contrast-enhanced MR images taken for GKRS treatment planning demonstrating a meningioma (1.7 cc) arising from the left tentorial edge with marked compression of the pons.
Bottom panel: MR images taken 41 months after treatment demonstrating a 53% decrease in tumor volume (0.8 cc).
DISCUSSION
Tentorial meningiomas comprise approximately 2-7% of intracranial meningiomas. Even histologically benign WHO grade I grade lesions may encase critical cerebrovascular and neural structures. This is especially true of tentorial meningiomas which Yasargil first categorized according to their attachment to the tentorium.(24)
Microsurgical Resection
Surgery offers histological confirmation for diagnosis, reduction of mass effect, and possible cure if gross total resection is achieved. The primary goal of surgery is complete microsurgical removal of the tumor, including resection of its dural attachment and associated bone invasion when relevant. This continues to provide the best means to prevent recurrence.(16, 17) The achievement of a complete resection, however, is often limited by tumor location. Furthermore, with relatively high recurrence and residual rates, repeat resection may present a greater risk of complication. Meningioma recurrence rates after macroscopic total resection were first described by Simpson in 1957.(17) At 5, 10 and 15 years following excision of tumor, its dural attachment and any abnormal bone, recurrence rates are reported between 5-8, 10-20, and 30-32%, respectively.(16, 17, 19) The natural history of these tumors is poorly predictive of the time from the first operation that a meningioma may recur or progress. Growth may occur even after a long period of time (i.e. >10 years).
Our main presenting signs and symptoms of patients with tentorial meningiomas were similar to those of other series with headache, cranial nerve palsies, and gait disturbance being common.(1, 11, 25) The main clinical goal of surgery is return of function for the patient and resolution of these deficits. A retrospective study by Bassiouni et al. looked at 81 patients treated microsurgically for tentorial meningiomas.(11) At the end of their mean follow-up period (5.9 years, ranging from 1 to 13 years), 87% of patients returned to normal life activity, 8% returned to their previous activity level but had a major deficit, and 5% were severely disabled and required permanent assistance. Two smaller studies reported similar functional outcomes. Out of 27 patients with mean follow-up of 30 months, 85% of patients returned to their previous activity level with either no or minimal symptoms, 11% returned to previous activity level with major cranial nerve palsy, and 4% patient required permanent assistance.(22) A series of 25 patients with mean follow-up of 5.3 years reported 76% with good neurological recovery, 4% with moderate disability, and 16% who died.(18)
Prior to the 1980’s, mortality rates following resection of tentorial meningiomas ranged from 16 to 44%. (13, 14, 28, 29) The advent of microsurgery and refined surgical approaches witnessed a reduction of postoperative mortality though not its elimination. Studies from the 1980’s through 1990’s reported mortality rates of 2.7 to 9.8%.(3, 5, 12, 27) The more recent Bassiouni series demonstrated 2.5% mortality.(11) Their deaths were attributed to intractable brain edema likely caused by deep venous injury after resection of a medial infratentorial meningioma and infarction of the pons after resection of a paramedian infratentorial meningioma with brainstem infiltration. Notably in the later decades of the last century, postoperative complications were described in as many as 19 to 34% of patients.(3, 12) Common postoperative complications of tentorial meningioma resection include cranial nerve deficits, hemiparesis, aphasia, cerebrospinal fluid (CSF) fistulae, and air embolism. Bassiouni et al. reported the following postoperative complications: 10% new cranial nerve deficit (50% permanency), 7% hemiparesis (40% resolution), 7% CSF fistulae (60% required permanent shunting), 4% air embolism (with no sequelae), 1% injury to transverse sinus (with no postoperative deficits), and 1% permanent cortical blindness. In another study of 14 patients with meningiomas of the falco-tentorial junction, one patient suffered permanent homonymous hemianopsia and one other trochlear paralysis. (20) Hashemi et al. described a rate of 9.5% new transient neurological deficits found postoperatively of which 33% retained their deficit permanently.(21) Even with a decline in mortality rates, microsurgery still has significant risks that must be weighted against likely benefits.
Stereotactic Radiosurgery
Over the past two decades, stereotactic radiosurgery has come to occupy an increasingly important position in the management of patients with meningiomas. To be certain, radiosurgery is not the preferred option for all meningioma patients, but it is either the primary or secondary treatment for many patients in the modern era of neurosurgery. For asymptomatic patients, radiosurgery has been used to treat small- to moderately-sized tentorial meningiomas that have been radiologically identified and diagnosed as likely benign, grade I neoplasms. Due to the neuroanatomical challenges of a gross total (i.e. Simpson grade I) resection of meningiomas in the tentorial region and the favorable benefit to risk profile of stereotactic radiosurgery, a maximal, safe resection followed by radiosurgery has become a common combined approach.
From 1989 to 2006, 752 patients with intracranial meningiomas were treated with GKRS at our institution. Of these, 35 tumors were WHO grade I tentorial meningiomas and included in this study. These patients were followed clinically and radiologically for an average of 5 years (range 2-16 years). This is significantly longer than previously published series where the average follow-up interval was 3 years (range, 1±8 years). (8, 25) Tumor parameters, GKRS planning and parameters in our study are comparable to current literature for radiosurgically treated tentorial meningiomas.(8, 25)
On imaging at the end of our follow-up period, 54% of tumors displayed a decrease in volume, 34% no change, and 11% an increase. This yielded an overall tumor control rate of 89%. We calculated our progression free survival to be 96%, 91%, and 73% at 3, 5, and 10 years, respectively. At the last clinical follow-up, 94% of patients demonstrated no change or improvement in their neurological condition and 6% worsened which was in accordance with other reported series. (11, 12, 3) When reviewing the literature, tumor control rates with radiosurgery for patients with grade I meningiomas of all locations combined are quoted in excess of 85% for most large series.(8) Similarly high tumor control rates are quoted in most large series looking at meningiomas of the skull base and convexities. (8) Results specific to GKRS for tentorial meningiomas are sparse. In 1998 Flickinger et al. reported 98% tumor control rate amongst 41 patients with tentorial meningiomas.(25) At the end of their average follow-up of 3 years, imaging studies showed 44% of tumors reduced in size, 54% displayed no change, and 2% increased. Clinically, their outcomes were similar with 95% of patients having clinical improvement or remaining stable and 5% deteriorating.
Complications related to radiosurgery for meningiomas are infrequent early after treatment. Overall there is a reported complication rate of 3–40% of cases with most rates in the range of 8%, 3% being transient and 5% being permanent.(8) Occasionally patients may experience headache or nausea immediately post treatment, which often resolve without any treatment. In the instance of frame-based stereotactic units, pin site infections remain very rare. Long-term complications include cranial nerve dysfunction, neurological deficits associated with adverse radiation effects (such as edema and necrosis), and radiosurgery induced neoplasia. Cranial nerves in proximity to skull base meningiomas are most commonly affected while cranial nerves in the cavernous sinus tend to be more radioresistant.(8) This may be based on tolerances to radiosurgery inherent to each cranial nerve. Nicolato et al. noted an 8% incidence of delayed complications in their 50 patient series which included edema and radiation necrosis. (35) Of the two patients in the Flickinger series who experienced poor clinical outcomes, one patient developed hemiparesis seen 9 months after irradiation, and the decline was attributed to higher tumor margin dose to the brainstem.(25) This patient’s symptoms and irregular imaging findings along the lateral brainstem resolved after corticosteroid therapy. Radiosurgery-induced neoplasia has such a low reported incidence that it is not even above the natural incidence of cancer in the general population.(37, 38) While the risk of radiosurgery-induced secondary tumor is very low, it still must be weighed in the treatment of patients with benign tumors and a long life expectancy.
Although radiosurgery is not suitable in all cases, it remains a valuable option for many. Flickinger noted that the selection of a patient with a tentorial meningioma for GKRS requires evaluation of age, neurological deficits, tumor location, rapidity of tumor growth and the general medical condition of the patient.(25) Radiosurgery is a reliable alternative or adjuvant to surgery for patients with small tumors of average tumor diameter, those with no appreciable mass effect, those diagnosed early in their evolution where the risks of surgery outweigh benefits in asymptomatic patients, those with small residual tumors despite microsurgical resection, those who are poor surgical candidates based on age or medical status, and those who decline microsurgical resection. Tentorial meningiomas in their close relationship or adherence to cranial nerves, brainstem, or neurovascular structures likewise may be managed with radiosurgery.
CONCLUSION
Gamma Knife radiosurgery affords a high rate of local tumor control and neurological preservation in patients with tentorial meningiomas. Nevertheless, temporary or permanent side effects as well as tumor progression can arise after radiosurgery. Long-term follow up should be performed after stereotactic radiosurgery.
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