Meningioma is a common intracranial tumor, accounting for approximately 13% to 26% of intracranial tumors. According to WHO 2007 edition classification, atypical meningioma (atypical, meningioma) and mesenchymal meningioma (anaplastic, meningioma) have poor biological behavior, atypical meningioma belongs to WHO grade II and mesenchymal meningioma is WHO grade III. In this paper, we review a total of 18 cases of atypical meningioma and mesenchymal meningioma admitted to our department from 2001 to 2006, and review the relevant literature.
Data and methods.
1. General data: 18 patients, 4 of whom had multiple surgeries in our hospital, for a total of 23 surgeries. There were 7 male cases and 11 female cases. The mean age of first onset was 46.2 in males, 56.6 in females, and 53.13 in females. clinical symptoms were mainly symptoms of cranial hypertension caused by intracranial occupancy, symptoms of functional area involvement and epilepsy, including headache and dizziness with or without vomiting in 11 cases, decreased muscle strength and sensory impairment of limbs in 7 cases, simple partial seizures in 4 cases, and ocular involvement in 6 cases, mostly decreased visual acuity and Some patients may have signs of cranial hypertension such as optic papillary edema and poorly defined borders. In addition, patients who had multiple surgeries could have surgical sequelae, such as facial palsy in 3 cases, damage to the articular nerve in 2 cases, and limited eye abduction in 1 case. Four tumors were located in the pterygoid crest, two originated in the canopy, one was a cranio-orbital communicating tumor, one was located in the trigeminal ventricle, and the other 10 were located in the hemispheric convexity, four of which were parsagittal sinus tumors and one in the central region. The recurrent tumors in patients with multiple surgeries were all located in the periphery of the original surgical field, and no distant metastasis was seen.
2. Imaging manifestations: CT showed an isometric or hypointense occupying shadow, mostly round, with scattered high-density calcified shadows in some of them, with poorly defined borders and edema in the periphery. The lesion is obviously enhanced. MRI shows T1, T2 iso- or iso-hyper-signal occupying shadow, mostly lobulated or with nodular protrusion, with poorly defined borders and peripheral edema bands. In some cases, it invades the cavernous sinus, superior sagittal sinus and peripheral skull. A few lesions may show cystic changes.
3. Surgery: 23 surgeries were performed in total. Intraoperatively, the base of the tumor was located in the dura mater, and the base was mostly wide with clear borders. Some of the tumors could be seen to invade the soft meninges and peripheral tissues with adhesions. The tumors were mostly dark red or flesh-colored with envelope, and the texture ranged from hard and tough to soft and brittle, with rich blood supply. The tumor is mainly extrusive to the surrounding brain tissues and neurovascular structures, but in some cases, the tumor encapsulates the cranial nerves and important blood vessels. 9 cases eroded the surrounding skull. The recurrent tumors are mostly located in the peripheral meninges of the original surgical field, multiple and small nodular. If the skull is defective, they can grow into the nearby muscles and form extracranial masses.
4. Pathological results: Pathological examination was performed on all 23 surgical specimens, including 9 cases of atypical meningioma (WHO grade II) and 14 cases of mesenchymal meningioma (WHO grade III). Microscopically, the tumor cells were arranged in swirls and bundles, the intertumor tissue was rich in blood vessels, and necrosis was visible within the tumor. The cells were densely arranged, shuttle-shaped, round, ovoid, with indistinct cytosolic boundaries, lightly stained cytoplasm, ovoid, short shuttle-shaped, darkly stained nuclei, and many nuclear fission phases. Occasionally, tumor giant cells were seen, with a large number of intracellular vacuoles and localized microcysts of various sizes. Some of the sacs were found to have light red-stained material. Most of them invade the meningeal tissue and the surrounding bone.
5. Statistical treatment: the survival rate of atypical meningioma and mesenchymal meningioma at 2 years after surgery, the recurrence rate at 2 years after complete resection and partial resection were compared, and t-test was performed.
Results.
1. degree of surgical resection and complications: out of 23 operations, 12 achieved Simpson, grade I resection, 6 Simpson grade II, 1 Simpson grade III, and 4 Simpson grade IV. One case had apnea due to posterior group cranial nerve palsy, three cases had cerebrospinal fluid nasal leakage, three cases had intracranial infection, one case had brain herniation due to occipital lobe infarction on the first postoperative day and underwent internal decompression surgery, the other two cases had cerebrospinal fluid leakage combined with intracranial infection on the 10th postoperative day and gave up treatment, and the other two cases formed after continuous drainage of the lumbar pool and antibiotic treatment. One case developed a grand mal seizure.
2. Follow-up: Except for 2 cases that died within half a month after surgery due to complications (intracranial infection and gastrointestinal bleeding) and 2 cases that were lost to follow-up, the remaining 14 patients were followed up for 24 to 72 months for a total of 19 operations. At 2 years postoperatively, the survival rate for atypical meningiomas was 86% (6/7) compared with 67% (8/12) for mesenchymal meningiomas, a significant difference. The recurrence rate 2 years after surgery in all cases combined was 70% (7/10) for partial resection and 30% (3/9) for complete resection, a significant difference.
Discussion.
Benign meningiomas account for approximately 13% to 26% of intracranial tumors, whereas the incidence of nonbenign meningiomas is lower, with atypical meningiomas accounting for approximately 5% to 7%, and mesenchymal meningiomas for 1% to 2.8%. The incidence of benign meningiomas differs significantly by gender, with a female prevalence in adult patients and a male:female incidence of 2:3 or 1:2. However, for non-benign meningiomas, previous studies have suggested that they appear to be more common in males and are thought to be associated with a higher proliferation index in men with meningiomas. However, in the present group of cases, the male-to-female ratio was 7:11, which is close to the incidence ratio of benign meningiomas.
Ten cases (56%) in this group were located on the convex surface, which is basically consistent with the literature, but still 7 cases (39%) involved the skull base to varying degrees, largely increasing the difficulty of complete surgical resection. The clinical manifestations of meningioma are mainly symptoms of cranial hypertension due to intracranial occupancy, such as headache and loss of vision, in addition to specific neurological dysfunction due to the impact of the tumor on the peripheral important neural structures, such as mild hemiparesis, epilepsy, aphasia, and cranial nerve injury. rockhill et al. reviewed 14 cases of malignant meningioma and found that 36% of them had headache and 43% of them had mild hemiparesis. In our group, mild hemiparesis was found in 39% of the cases, and headache and dizziness increased in 61% of the cases.
CT and MRI are still the most commonly used imaging tests to diagnose meningiomas, but these two tests are difficult to differentiate between benign and non-benign meningiomas. Previous reports suggest that edema, lack of calcification, bone destruction, and cystic changes are characteristic of non-benign meningiomas, but similar presentations are seen in many benign meningiomas. Currently, the imaging of non-benign meningioma is considered to have the following characteristics: (1) no calcification; (2) mushroom-like or lobulated; (3) non-homogeneous enhancement; (4) central necrosis; and (5) indistinct tumor margins. Since non-benign meningioma grows fast and easily invades the surrounding brain tissue and skull, combined with the cases in this group, we believe that when MRI reveals a lobulated meningioma with unclear borders, disappearance of the arachnoid space, wide meningeal base, obvious destruction of the surrounding skull but not cranial thickening, or even extra-cranial foci, it strongly suggests that the meningioma is of poor nature. Buhl et al. found a characteristic lactate peak in preoperative MRI spectral analysis in more than 63% of atypical meningiomas, which may help in the differentiation.
Surgery remains the treatment of choice for atypical meningiomas and mesenchymal meningiomas. Even if recurrence occurs, reoperation should still be considered as long as the patient’s condition permits. The ultimate goal of meningioma surgery is complete resection of the tumor along with removal of the involved dura and skull. In our group, we found that the recurrent tumors originated in the meninges surrounding the original surgical field; therefore, we believe it is more important to emphasize the need to maximize the removal of the so-called “normal meninges” surrounding the tumor during the first surgery. According to Simpson’s criteria for meningioma resection, a level I resection, i.e., a complete resection, involves the removal of 2-4 cm of the surrounding meninges and the affected skull. Dziuk et al. reviewed 28 cases of fully resected and 20 cases of partially resected atypical meningiomas and mesenchymal meningiomas and found that the 5-year remission rate after complete resection was 39%, while partial resection was 0. Palma et al. also found that the clinical course of patients with simpson’s and grade I resection was significantly better than that of patients with grade II and III resection. Although the number of cases in this group is small, it is also evident that the 2-year recurrence rate of complete resection is significantly lower than that of partial resection.
Meningiomas at the base of the skull mostly invade or encase important structures such as cavernous sinuses, cranial nerves, and large blood vessels, and excessive pursuit of complete resection inevitably damages these structures during surgery. Jääskeläinen reported that the 5-year recurrence rates of atypical meningioma and mesenchymal meningioma were still 38% and 78%, respectively, after complete resection, while Perry et al. found that the 5-year recurrence rates of atypical meningioma and mesenchymal meningioma were 41% and 41%, respectively, after complete resection. The recurrence rate was 41% for atypical meningiomas and 56% for mesenchymal meningiomas. Therefore, for non-benign meningiomas at the skull base, a detailed preoperative evaluation should be performed to avoid surgical complications that may seriously affect the patient’s quality of life. In order to better assess patients’ postoperative behavior, Morales et al. graded skull base meningiomas according to the number of nerves and blood vessels encapsulated by the tumor. Grade 1 is when the tumor encapsulates only one nerve or blood vessel; grade 2 is when the tumor encapsulates one nerve or two major arteries; and grade 3 is when the tumor encapsulates more nerves and blood vessels. The evaluation of 85 patients according to this grading revealed that 98.5% of grade 1 patients achieved total resection and 96% of patients had a postoperative Karnofsky, behavioral score (KPS) of at least 70. only 83% of grade 2 patients achieved total resection and only 70% had a KPS of 70, while only 43% of grade 3 patients achieved total resection and had a lower KPS score.
Goldsmish reported a 5-year survival rate of 58% and a 5-year remission rate of 48% in 23 cases of atypical meningioma and mesenchymal meningioma treated with conventional fractionated radiotherapy after partial resection, and the authors concluded that radiotherapy at doses above 53 Gy was more effective and that early postoperative radiotherapy was more effective. Dziuk also found that early postoperative conventional radiotherapy resulted in 80% remission compared to 15% without radiotherapy. And for recurrent atypical meningiomas and mesenchymal meningiomas, the proportion of 2-year remissions was 89% in the radiotherapy group compared to 50% in the no-radiation group. However, there was no difference between the two groups at five years.
Stereotactic radiotherapy is now increasingly used in the treatment of neurosurgical tumors and is also effective for atypical and mesenchymal meningiomas. Hakim et al. performed early stereotactic radiotherapy at 15 Gy in 26 cases of atypical meningiomas and 18 cases of mesenchymal meningiomas, and the mean remission periods were 24.4 and 13.9 months, respectively, with 3-year survival rates of 83.3% and 43.1%, respectively. Harris et al. also found that early postoperative stereotactic radiotherapy resulted in 5-year remission rates of 83% and 72% for atypical and mesenchymal meningiomas, respectively. However, it should be noted that the above authors emphasized early postoperative radiotherapy and pointed out that since stereotactic radiotherapy mainly targets nodal lesions, such as residual tumors in the cavernous sinus, it is difficult to treat tumor cells infiltrating the peripheral brain tissue and dura mater, so conventional radiotherapy in the operative field is still necessary. To date, there is no clear evidence to confirm the effectiveness of pharmacological treatments such as mifepristone, hydroxyurea, vincristine, and adriamycin for non-benign meningiomas.
The prognosis of atypical meningioma and mesenchymal meningioma is often poor, with Perry et al. reporting a mean survival time of 1.5 years and a 5-year survival rate of 68% for mesenchymal meningioma, while atypical meningioma is similar to benign meningioma with a mean survival time of 10-14 years and a 5-year survival rate of 25%. Perry et al. concluded that onset under 40 years of age, male patients, and tumor location at the skull base suggested a poor prognosis. Subsequent literature further suggested that partial resection, primitive cells, 20 mitotic phases/10 high-powered views, and nuclear anisotropy were pathologically suggestive of poor prognosis.
Cases of malignant transformation of benign meningiomas have been reported in the previous literature; Jääskeläinen et al. analyzed 70 recurrent benign meningiomas and found that 10 of them were malignant, and Palma et al. also reported that 6 of 23 recurrent atypical meningiomas (26%) progressed to mesenchymal meningioma. In our group, there were also 2 cases of further malignant transformation from atypical meningioma to mesenchymal meningioma, suggesting the potential for further biological deterioration of meningioma.