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Parasagittal meningiomas: follow-up review
Surgical Neurology 66 (2006) S3:20 – S3:28 www.surgicalneurology-online.com
Meningioma
Parasagittal meningiomas: follow-up review Benedicto Oscar Colli, MD, PhDa,4, Carlos Gilberto Carlotti Jr, MD, PhDa, Joa˜o Alberto Assirati Jr, MDa, Marcius Benigno Marques dos Santos, MDa, Luciano Neder, MD, PhDb, Antonio Carlos dos Santos, MD, PhDc a
Division of Neurosurgery, Department of Surgery, bDepartment of Pathology, and cDivision of Radiology, Hospital das Clinicas de Ribeira˜o Preto, Ribeira˜o Preto Medical School, University of Sa˜o Paulo, Ribeira˜o Preto, Sa˜o Paulo, Brazil Received 29 June 2006; accepted 2 August 2006
Abstract
Background: Parasagittal meningioma is one that fills the parasagittal angle, with no brain tissue between the tumor and the SSS. Invasion of the SSS is a challenge for complete removal and, consequently, for recurrence of these tumors. The objective of this study was to analyze the factors that influenced the clinical outcome of patients with parasagittal tumors surgically treated. Methods: Review of data on 53 patients with diagnosis of parasagittal meningiomas surgically treated from 1984 to 2004. Thirty-four (64.2%) were female and 19 (35.8%) were male; age ranged from 18 to 81 years old (mean, 54.98 F 5.80). Follow-up ranged from 2 to 261 months (mean, 93.71 F 68.45). The patients were operated on using microsurgical techniques. Tumors in the anterior third (9) or occluding the SSS (5) were removed with the sinus; tumors touching/pouching the SSS (20) were removed and its dural attachment coagulated; tumors invading one sinus wall (10) were removed with partial excision and reconstruction of the sinus wall, and tumors invading more than one sinus wall in the posterior two thirds of the SSS (7) had a subtotal removal. No attempt at sinus resection and reconstruction was performed for tumors placed in the posterior two thirds of the SSS. Analysis of the patient outcome was done using survival and RFS Kaplan-Meier curves. The v 2, Fisher exact, log-rank, Mann-Whitney, and Kruskall-Wallis ANOVA tests were used for comparing demographic data, survival curves, proportions, and medians, respectively. Results: Total and subtotal resection were achieved in 85% and 13.1%, respectively. Males had better survival than females ( P = .0252). Total RF rates were 10%, 25%, and 100% at 5 years and 100%, 50%, and 100% at 10 years for patients with meningiomas WHO grades I, II, and III, respectively. The RF survival curve was better for patients with grade I meningioma (grades I vs II vs III, P = .0001). There was no difference between the RF survival curves according to age, histopathologic WHO grade, location along or invasion of the SSS, and extent of resection. Males ( P = .0401), WHO grade I ( P b .0001), total resection ( P = .0139), and less sinus invasion ( P = .0308) had better RFS curves. Operative, surgery-related, and overall mortality were 1.9%, 5.4%, and 26.4%, respectively. Conclusions: Recurrence of parasagittal meningiomas predominated in males, in grades II/III tumors, after subtotal resection, and with more invasion of the SSS. Subtotal or total resections without sinus resection were considered adequate for treating these patients. D 2006 Elsevier Inc. All rights reserved.
Keywords:
Parasagittal meningiomas; Surgical treatment; Survival curves; Recurrence-free survival curves; Extension of resection
Abbreviations: ANOVA, analysis of variance; CT, computed tomography; KPS, Karnofsky Performance Scale; MR, magnetic resonance; RFS, recurrence free survival; SSS, superior sagittal sinus; WHO, World Health Organization. 4 Corresponding author. Departamento de Cirurgia, HCFMRP, Campus Universita´rio, USP, 14048-900 Ribeira˜o Preto, SP, Brazil. Tel.: +55 3602 2498; fax: +55 3602 2498. E-mail address: [email protected] (B.O. Colli). 0090-3019/$ – see front matter D 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.surneu.2006.08.023
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Table 2 Initial signs and symptoms in 51 patients with parasagittal meningiomas
1. Introduction Cushing and Eisenhardt [8] defined parasagittal meningioma as one that fills the parasagittal angle, with no brain tissue between the tumor and the SSS. Parasagittal meningiomas comprise 21% to 31% of intracranial meningiomas [6,8,13,15,28,29], and the distribution of the meningiomas along the SSS ranged from 14.8% to 33.9% in the anterior third, from 44.8% to 70.4% in the middle third, and from 9.2% to 29.6% in the posterior third of the sinus [8 -10,12]. Most parasagittal meningiomas are benign tumors that can be cured with surgical treatment. Nevertheless, despite the improvement in the diagnosis and topographic evaluation by CT scans and MR imaging, the involvement of the SSS and surrounding veins, specially for tumors located in the middle third of the SSS, may preclude their complete removal, making the management of these tumors a real challenge because of the relatively high mortality and morbidity [5,9,28]. The routine use of microsurgical techniques has reduced the surgical mortality, but the postoperative morbidity and rate of recurrence for these tumors remain high [9]. The objective of this study was to analyze factors that influenced the clinical outcome of a group of patients with parasagittal meningiomas treated at the Division of Neurosurgery of the Hospital das Clı´nicas, Ribeira˜o Preto Medical School, University of Sa˜o Paulo. 2. Clinical material and methods 2.1. Patient population Parasagittal meningioma cases comprised 19.24% (61) of 317 patients with a radiologic diagnosis of intracranial meningioma assisted from 1984 to 2004. The design of this study was a retrospective review of data on 53 consecutive patients with parasagittal meningiomas submitted to surgical treatment. Diagnosis of these tumors was performed using CT and/or MR imaging of the skull. Eight patients with radiologic diagnosis were conservatively treated (small and calcified tumors in aged patients or refused surgical treatment). According to the histopathologic WHO classification [16], 41 patients presented benign grade I meningiomas (16 transitional, 15 meningothelial, 4 psammomatous, Table 1 Summary of demographic data in 53 patients with parasagittal meningiomas Characteristic
Sex Female Male Female/male Age (y)4 Age range (y) Female Male
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Meningiomas
Total
Grade I
Grade II
Grade III
29 12 2.42:1 56.44 F 16.12
4 4 1:1 52.38 F 16.61
1 3 1:3 45.3 F 9.84
34 19 1.79:1 54.98 F 15.89
24-78 18-81
34-70 27-67
34 45-58
24-78 18-81
4 Values are presented as the mean F SD.
Signs and symptoms Generalized seizures Partial seizures Headache Hemiparesis Incidental Visual loss Behavior disturbance Monoparesis Disorientation Other 4
Location along the superior sagittal sinus Anterior third
Middle third
Posterior third
9 – 7 3 2 2 2
8 2 3 4 3 1 1 2 2 1
2 – – 1 1 1 – – – 1
1
4 These signs and symptoms included apathy, drowsiness, dementia, depression, monoparesis, dysphasia, loss of initiative, and tremor in 1 patient with meningioma of the anterior third, and irritability, dysphasia, diplopia, agitation, urinary incontinence, dysphasia, hemianopsia, and ataxia in 1 patient with meningioma of the middle third of the superior sagittal sinus.
2 angiomatous, 3 fibroblastic, 1 secretory), 8 had grade II (6 atypical, 2 grade II hemangiopericytomas), and 4 grade III meningiomas. The hemangiopericytomas were included because they were not diagnosed previously and because they pose the same technical problems during surgery. 2.2. Clinical findings The most important demographic characteristics of patients are presented in Table 1. There was a female predominance in all patients (average female/male ratio of 1.8:1) and in patients with grade I meningiomas. The sex distribution was similar for patients with grade II meningiomas, and, despite the small number, there was a male predominance in patients with grade III meningiomas. Age ranged from 18 to 81 years old (mean, 54.98 F 15.89). There was no difference between the mean age of patients in Table 3 Signs and symptoms presented at the diagnosis in 51 patients with parasagittal meningiomas Signs and symptoms Generalized seizures Partial seizures Headache Hemiparesis Incidental Visual loss Behavior disturbance Aphasia/dysphasia Monoparesis Disorientation Other 4
Location along the superior sagittal sinus Anterior third
Middle third
Posterior third
9 – 7 4 3 3 2 1 1 1
10 2 6 4 3 1 1 4 3 2 1
2 – – 1 1 1 – – – 1
4 These signs and symptoms included apathy, ataxia, dizziness, pyramidal signs, drowsiness, dementia, depression, loss of initiative, tremor, coma, and hemiparesis in 1 patient with meningioma of the anterior third; irritability, diplopia, agitation, urinary incontinence, hemianopsia, pyramidal signs, mental confusion, ataxia, and difficulty in walking in 1 patient with meningioma of the middle third; and ataxia and dizziness in 1 patient with meningioma of the posterior third of the superior sagittal sinus.
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2.4. Functional outcome
Fig. 1. Survival curve for patients with parasagittal meningiomas according to sex. Significant difference ( P = .0252, df = 1 [log-rank test]).
relation to the histopathologic type of tumor and considering grades I vs II and III ( P = .5413, 5 groups [Kruskall-Wallis nonparametric ANOVA]). The clinical signs and symptoms at onset and at diagnosis, according to the location along the SSS, and the average duration of symptoms are summarized in Tables 2 and 3. Follow-up ranged from 2 to 261 months (mean, 93.71 F 68.45; median, 78.0). Twenty-four (45.3%) were placed in the anterior third of the SSS, 26 (49.1%) in the middle, and 3 (5.6%) in the posterior third of the sinus. 2.3. Management of the disease 2.3.1. Surgical treatment The patients were operated on using microsurgical techniques and special attention was given to the preoperative evaluation of the permeability of the SSS and of the location of parietal veins using digital angiography and, more recently, MR imaging angiography. Nine patients (6 grade II, 3 grade III meningiomas) underwent adjuvant conventional radiotherapy. No attempt at complete sinus resection followed by reconstruction was performed when the tumor was placed in the posterior two thirds of the SSS. The extent of resection was assessed macroscopically during surgery and postoperatively using CT or MR imaging 48 hours and 6 months after operation (radical removal when there was no evidence or doubt about residual tumor in the MR image; subtotal when the resection was N 90%; and partial when the resection was b 90%). Forty-five (85%) patients had radical tumor resection, 7 (13.1%) had subtotal resection, and 1 (1.9%) had partial resection but died during surgery. The follow-up median for patients who underwent radical or subtotal resection was not significantly different ( P = .3287, Mann-Whitney U test). All patients with WHO grades II and III meningiomas had initial total resection. Based on intraoperative findings, invasion of the SSS could be classified [5] in 37 (69.8%) patients with tumors types I to IV (sinus permeable) and in 16 (30.2%) with types V to VIII (sinus almost/completely occluded).
Because of the small number of patients with grades II and III tumors and with tumors in the posterior third of SSS, analysis of outcome was performed comparing patients with tumors in the anterior vs middle third and patients with histopathologic grades I vs II to III meningiomas. The preoperative, postoperative (first 10 days), and follow-up outcome were analyzed using the KPS to measure the degree of disability. Patients were classified into 1 of 3 groups. (1) Those with normal function or minimal symptoms and can work (KPS score, 80-100); (2) those who are independent but cannot work (KPS score, V 70); and (3) those with moderate or severe disability (KPS score, V 50). For patients who experienced tumor recurrence and consequent clinical deterioration, the best KPS score obtained during the follow-up course was used. For patients who died during the immediate postoperative course, the KPS score acquired before death was used to indicate both the immediate postoperative and follow-up scores. Three patients did not attend 6 months of follow-up and did not receive a KPS score at this time. Follow-up analysis was performed using the KaplanMeier survival and RFS curves and rates in relation to sex, age, histopathologic grade, location of tumor, extent of resection, and invasion of SSS. Nine patients with tumors in the anterior third and 5 patients with the middle/posterior third of the SSS occluded by the tumor were excluded from the last analysis because the sinus was removed en bloc with the tumor. 2.5. Statistical analysis Statistical analysis was performed using the v 2 and the Fisher exact tests for comparing proportions; the MannWhitney U test and the Kruskall-Wallis nonparametric ANOVA for comparison of medians; and the log-rank test for comparison of survival curves and rates. An a error probability not exceeding 5% was considered significant for 2-tailed probability tests. The tests were performed using
Fig. 2. Recurrence-free survival curve for all patients with parasagittal meningiomas according to sex. Significant difference ( P = .0401, df = 1 [log-rank test]).
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Fig. 3. Recurrence-free survival curves for patients with parasagittal meningiomas according to the WHO histopathologic grades. Significant difference ( P b .0001, df = 2 [log-rank test]).
GraphPad PRISM (version 3.0; GraphPad Software, Inc, San Diego, CA, USA).
3. Results 3.1. Follow-up review 3.1.1. Survival Fig. 1 presents the survival curves for all patients according to sex. The 5-year survival estimates were 93.7% and 79.3%, and the 10-year survival estimates were 79.8% and 35.3% for female and male patients, respectively. The survival curve was better for females ( P = .0252, df = 1 [log-rank test]). There was no significant difference (log-rank test) for the survival curves according to sex for patients with grade I meningiomas ( P b .2291, df = 1); according to histopathologic grades I, II, and III ( P = .4557, df = 2) and subtypes of grade I ( P b .3751, df = 3), according to the location along the SSS (anterior vs posterior two thirds) for all patients ( P b .5204, df = 1) and for patients with grade I meningiomas ( P b .1544, df = 1); and according to the invasion of the SSS (grades I-IV vs grades V-VIII [5]) for all patients ( P b .4197 [log-rank test]) and for patients with WHO grade I meningiomas ( P b .4737 [log-rank test]). 3.1.2. Recurrence-free survival Total recurrence rate at follow-up was 32.7% (17 patients), distributed in 17.5% (7 patients), 75% (6 patients), and 100% (4 patients) of patients with WHO grades I, II, and III meningiomas, respectively. There was significant difference (Fisher exact test) between the rates for patients with WHO grades I and II ( P = .0033, df = 1), and between grades I and III ( P = .0027, df = 1), and no significant difference between grades II and III ( P = .5152, df = 1). The RF rates were 80.8%, 71.4%, and 0% at 5 years, and 67.5%, 17.9%, and 0% at 10 years for patients with grades I, II, and III meningiomas, respectively. Total RF rates were
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27.6% at 5 years and 47% at 10 years. Recurrences for all patients occurred in the first 5 years in 10 patients (58.8), after 5 years in 7 (41.2%), and after 10 years in 2 (11.8%) (at 127 [atypical meningioma] and 144 [hemangiopericytoma] months). Among patients with WHO grade I meningiomas, recurrence occurred in 4 (57.1%) patients in the first 5 years and in 3 (42.9%) between 5 and 10 years. Fig. 2 presents the RFS curves for all patients according to sex. The 5-year RF estimates were 83.7% and 63.2%, and the 10-year survival estimates were 69.8% and 14.7% for female and male patients, respectively. Recurrence-free survival curve was better for females than for males for all patients ( P = .0401, df = 1 [log-rank test]). There was no significant difference (log-rank test) for the RFS curves according to sex for patients with grade I meningiomas ( P b .1209, df = 1) and according to age (10-29 vs 30-39 vs 40-49 vs 50-59 vs 60-69 vs 70-90 years old, P b .3344, df = 4 [log-rank test] and 10-49 vs 50-90 years old, P b .2800, df = 1) for all patients. The RFS curves according to histopathologic classification are presented in Fig. 3. The 5-year RFS estimates were 80.8%, 67.5%, and 0%, and the 10-year survival estimates were 67.5%, 11.4%, and 0% for patients with grades I, II, and III meningiomas, respectively. The RFS curve was better for grade I than for grades II and III ( P b .0001, df = 2 [log-rank test] and P b .0001, df = 1 [log-rank test for trend]). The medians of the RFS curves were also different ( P = 0001, df = 2 [Kruskall-Wallis–ANOVA]). They were significant (Dunn multiple comparisons posttest) for grades I and II ( P b .05), and for grades I and III, and not significant for grades II and III ( P N .05). Patients with grade I tumors had less recurrence than those with grades II and III tumors. The RFS curves for patients with grade I tumors were not significantly different ( P b .3537, df = 3 [log-rank test]) according to their histopathologic subtypes. The RFS curves for all patients and for patients with grade I tumors according to the extent of resection (radical vs subtotal) are depicted in Figs. 4 and 5. Radical resection allowed better RFS curve (log-rank test) than subtotal for all
Fig. 4. Recurrence-free survival curves for all patients with parasagittal meningiomas according to the extension of resection. Significant difference ( P b .0139, df = 1 [log-rank test]).
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Fig. 5. Recurrence-free survival curves for patients with WHO grade I parasagittal meningiomas according to the extent of resection. Significant difference ( P = .0305, df = 1 [log-rank test]).
patients ( P b .0139, df = 1) and for patients with grade I meningiomas ( P = .0305, df = 1). Fig. 6 presents the RFS curves for all patients according to the location along the SSS (anterior vs middle/posterior third). The RFS curve was better (log-rank test) for patients with tumor in the anterior third of the SSS ( P b .0112, df = 1), but it was similar for patients with grade I meningiomas ( P b .1544, df = 1 [log-rank test]). The RFS curves for all patients and for patients with WHO grade I meningiomas in relation to the extension of invasion of the SSS (Bonnal and Brotchi grades I-IV vs V-VIII) are depicted in Figs. 7 and 8, respectively. The curves were better (log-rank test) for less invasion of the SSS for all patients ( P b .0308, df = 1 [log-rank test]) and for patients with grade I meningiomas ( P b .0301, df = 1).
Fig. 7. Recurrence-free survival curves for all patients with parasagittal meningiomas according to the invasion of superior sagittal sinus [5]. Significant difference ( P b .0308, df = 1 [log-rank test]).
One patient with type 2 neurofibromatosis and multiple meningiomas (grade I) died during her seventh surgery after circulatory shock due to massive hemorrhage. Two patients (grades I and II) died 2 months after surgery because of
postoperative complications (pulmonary infection and pulmonary embolism after deep venous thrombosis), and 11 patients died during the follow-up period (operative mortality, 1.9%; surgery-related mortality, 5.7%; and overall mortality, 26.4%). During the follow-up, 3 deaths were due to progression of grade III meningiomas and 8 deaths were not related to the tumor (6 grade I tumors, 1 grade II, 1 grade III). The age of these patients ranged from 65 to 88 years old (65, 70, 73, 77, 82, 85, and 88; mean, 77.14; SD, F8.355). Two patients (grade I) developed postoperative monoparesis, 1 patient (grade II) developed tetraparesis, and 1 (grade I) developed crural paraparesis, totaling 4 (7.8%), 1 permanent and 3 transient, all of them located in the middle third of the SSS. Two patients (3.9%) developed osteomyelitis treated with removal of the flap and later cranioplasty, 4 (3.9%) had a subgaleal collection treated with aspiration, and 1 (1.9%) had a fluid collection over a bovine pericardial graft, detected on a control CT; this collection was conservatively treated and became calcified. Nonneurologic complications observed were venous thrombosis in 2 (3.9%)
Fig. 6. Recurrence-free survival curves for patients with parasagittal meningiomas according to the location along the superior sagittal sinus. Significant difference ( P b .0112, df = 1 [log-rank test]).
Fig. 8. Recurrence-free survival curves for patients with WHO grade I parasagittal meningiomas according to the invasion of the superior sagittal sinus [5]. Significant difference ( P b .0301, df = 1 [log-rank test]).
3.2. Mortality and morbidity
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Table 4 Preoperative, postoperative, and follow-up functional status Functional status
KPS score Preoperative
Immediate postoperative
Follow-up
WHO histopathologic grade Grade I No. of patients Normal or minimal 80-100 symptoms and working Independent, 70 not working Moderate or 50 severe disability
Grades II/III Total
41 12 30 (56.6%) 5 (9.4%)
9 (17%) 2 (3.8 %)
7 (1.3.2%) –
53 35 (66%)
Grade I
Grades II/III Total
40 12 35 (57.7%) 5 (9.6 %)
Grade I
Grades II/III Total
52 39 11 40 (76.9 %) 33 (66%) 5 (10%)
50 38 (76%)
16 (30.2%)
4 (7.7 %)
5 (9.6%)
9 (17.3%)
3 (6%)
4 (8%)
7 (14%)
2 (3.8%)
1 (1.9 %)
2 (3.8%)
3 (5.8%)
3 (6%)
2 (4%)
5 (10%)
patients (1 followed by fatal pulmonary embolism) and fatal pulmonary infection in 1 (1.9%) patient. 3.3. Postoperative functional outcome Preoperative, immediate postoperative, and follow-up functional disabilities assessed by KPS are presented in Table 4. The scores were similar (v 2 test, df = 2) in all evaluations ( P = .3274 for all patients, P = .2110 for patients with grade I tumors, and P = .9781 for patients with grades II-III tumors). Preoperatively, 18 (34%) patients had KPS scores of 70 or less, and, postoperatively, 12 (23.1%) had scores of at least 70 (no significant difference, P = .2809, Fisher exact test, df = 1). Four (7.7%) patients experienced deterioration postoperatively (KPS, V 70) and 7 (13.4%) experienced improvement (KPS, z 80). Assessment at 6 months demonstrated 1 additional patient (grade I) with KPS score of 70 or less. 4. Discussion
the sinus (primarily or with a graft). Tumor invading only the external layer of the lateral sinus wall can be completely resected by laminating the external layer of the tumor and preserving the internal layer of the sinus wall. Primary closure of the SSS can be accomplished for tumor invading the lateral angle of the sinus. The piece of tumor attached to the sinus can be resected followed by a progressive running suture along the sinus wall. During this resection, blood flow should be interrupted with vascular clamps, forceps, or with finger compression to prevent air embolism. When some perforations occurred in the sinus wall during resection, we used a flap from the falx [21], rotated upward, and sutured anteriorly, posteriorly, and superiorly to reconstruct the lateral wall of the sinus. Resection and reconstruction of the sinus are feasible, but they may be followed by significant morbidity [5,11]. In our series, we opted to perform a subtotal resection when the posterior two thirds of the sinus was significantly invaded by a tumor and we never interrupted and reconstructed the sinus.
4.1. Surgical treatment
4.2. Survival
The treatment of parasagittal meningiomas is predominantly surgical. Besides major hemorrhage from the scalp, bone, dura, tumor, and sinus, the attachment to the dura, sinus, or falx makes it more difficult to remove the tumor and increases the chance of injury to the normal brain. Invasion of the sinus is a major problem in the resection of these tumors. It is a general concept that the anterior third of the SSS may be resected without sequelae [5,23], but resection of the posterior two thirds of the sinus may cause severe, permanent damage to the adjacent brain if the sinus is patent. We observed no morbidity or mortality that could be attributed to ligature of the anterior third of the SSS in 24 patients, which corroborates this concept. When the sinus is completely occluded, it may be resected without significant risks [5,9,23]. The surgeon has 3 options when the SSS is invaded: (1) leave a small portion of the tumor attached to the sinus and wait for the occlusion of the sinus by the tumor and for the development of collateral venous drainage to try a late complete resection; (2) resect the tumor to obliterate the sinus; or (3) resect and reconstruct the involved part of
Sex was the only significant variable for survival among patients with parasagittal meningiomas (better survival curve for females in relation to males). Other factors such as age, WHO histopathologic grades (grades I vs II vs III), the extent of resection (Simpson grades I/II vs grade IV; radical vs subtotal), location of the tumors along the SSS (anterior third vs middle and posterior third), and the extent of compromising of the SSS according to Bonnal and Brotchi [5] grades (I-IV vs V-VIII) for all patients and for patients with grade I parasagittal meningiomas were not significant for survival. 4.3. Recurrence Recurrence of parasagittal meningiomas occurs in 7.9% to 29% [3,6,9,13,22,26], and it is dependent on the extent of the follow-up (5%-17.7% at 5 years and in 14.4%-24% at 10 years) [6,9,10,22]. Recurrence rate in all the follow-up in our series was 32.7%, and it was 12% at 5 years and 16% at 10 years. Most authors agree that recurrence rates for patients with atypical or malignant meningiomas are greater than for patients with WHO grade I [1,2,13,19,20,24,27],
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and this is also true for patients with parasagittal meningiomas as demonstrated by Di Meco et al [9] and by our results. There was no patient with grade III tumor without recurrence at the 5-year follow-up. Among the subtypes of WHO grade I intracranial meningiomas, psammomatous tumors with a high density of calcification rarely recur [17], and the angioblastic meningiomas, even if they are separated from the hemangiopericytomas, seem to have a markedly high rate of recurrence [3,7,14]. Despite no significant difference among the histopathologic subtypes of WHO grade I tumors in our series, there was no recurrence among patients with psammomatous tumors. Delay in recurrence is variable among patients with intracranial meningiomas and it has been detected early after the routine use of follow-up CT scans [6]. Recurrence has been reported as more than half occurring by the end of the fourth/fifth year [22], and our results agree with these findings. Late (after 10 years) recurrence in our series (11.8% of the recurrences) was similar to that reported by others [22], but, interestingly, these recurrences occurred in patients with an atypical meningioma and a hemangiopericytoma. Many factors are reputed to influence the recurrence of all intracranial meningiomas. For some of them, this role is incontestable, but for others it is controversial. Regarding age and sex, some authors related that the risk is increased and the delay of recurrence is shorter in younger patients and that there is no difference in the recurrence between sexes for patients with any kind of intracranial meningiomas [4,22] and parasagittal meningiomas [9]. Simpson, in 1957 [26], established the recurrence of meningiomas according to the extent of resection, and since then other authors have confirmed his findings [6,9,13]. Recurrence at 5 years after tumor plus dural resections ranges from 5% to 16%, after total tumor resection from 11.9% to 18%, and after partial resection of the tumor from 14% to 41.9% [9,10]. Di Meco et al [9] reported no interference of tumor location along the SSS. In our series, age did not interfere with the recurrence rates. Females had less recurrence than males for all patients. The extent of resection influenced the decrease in recurrence rates for all patients with parasagittal meningiomas and for patients with WHO grade I meningiomas. Considering all patients, patients with tumors located in the anterior third of the SSS had significantly less recurrence than patients with tumors located in the middle and posterior third of the SSS, but there was no difference for patients with the subtypes of WHO grade I meningiomas. The extent of invasion of the SSS (Bonnal and Brotchi grades I-IV vs grades V-VIII) influenced positively the rates of recurrence for all patients and for patients with WHO grade I meningiomas. Despite a high recurrence rate in all the follow-up (32.7%), and the better RFS curves for radical resection in our series, if we consider that the recurrent rates were 12% at 5 years and 16% at 10 years and that more than half of the recurrences occurred in patients with WHO grades II and III tumors, we can consider that our results justify our less aggressive policy in relation to the resection of the SSS.
4.4. Mortality and morbidity Operative mortality for resection of parasagittal meningiomas varied from 1.85% to 12.3% [6,8,9,10,12,18]. Mortality is associated significantly with old age [25], is greater for patients with tumor located in the middle third of the sinus, and did not depend on the extension of the resection [9,10]. Di Meco et al [9] reported a decrease from 3.7% to 1.85% in operative mortality after the introduction of microsurgical techniques in the treatment of patients with parasagittal meningiomas operated on from 1986 to 2001. Causes of death among the patients of Giombini et al [10] were predominantly cerebral swelling, followed by pulmonary embolism, postoperative hematoma, cardiac failure, and bronchopneumonia. Predominance of cerebral swelling in patients with tumor in the middle third of the SSS probably indicates surgical damage to cortical veins closely related to the tumor. The operative mortality (first 30 days after surgery) observed in our series was 1.9%, the surgeryrelated mortality was 5.7%, and the overall mortality rate in the follow-up was 26.4%. Surgery-related deaths were caused by circulatory chock in 1 patient, by pulmonary infection in another, and by pulmonary embolism in a third patient. In the follow-up, 8 deaths were not related to tumor and 3 patients with grade III meningiomas died because of progression of the disease. Morbidity after resection of parasagittal meningiomas remains significant. Transient neurologic worsening in the immediate postoperative period was common (8.3%) among the patients of Di Meco et al [9] and was related to the great size of the tumor and to the location in the middle and posterior third of the SSS. The authors speculate that this impairment was caused by transitory venous engorgement and difficulties in venous drainage caused by sinus stenosis in the event of marginal resection. Neurologic recovery probably was favored by rearrangement of venous anastomosis and by opening of alternative venous outflow pathways that ultimately could restore the conditions of normal venous drainage. Other operative complications observed by the authors were intracranial hematomas (2 patients, 1.8%), subgaleal fluid collection in 11 (10%) patients (3 resolved spontaneously, 6 required lumbar puncture, and 3 required surgical treatment), wound infection requiring surgical treatment in 3 (2.7%), and new onset of seizures in 3 patients (7.7%). Nonneurologic complications included 3 (2.7%) deep venous thrombosis. We observed neurologic deterioration in 4 (7.8%) patients and it was permanent in one of them. All neurologic deterioration occurred in patients with tumors located in the middle third of the SSS. As these complications are generally caused by interruption of the SSS or by lesion of cortical veins draining to the SSS, every effort should be exerted to preserve the bridging veins located over or anterior or posterior to the tumor to avoid surgical interruption or inducing thrombosis of such veins which could lead to regional venous infarction with delayed neurologic deficit. Other complications observed were
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subgaleal collection, wound infection, and epidural collection. Systemic complications observed include venous thrombosis in 3.9%, which was responsible for the death of 1 patient. 4.5. Postoperative functional outcome As postoperative neurologic worsening is not uncommon, functional outcome sometimes may worsen after surgical treatment of parasagittal meningiomas. Di Meco et al [9] reported an immediate postoperative worsening of preexisting condition in 11.1% of cases and most of them improved sometime later, after the improvement of the neurologic deficit. In our series, 7.7% of patients had a worse immediate postoperative KPS than preoperatively, but 13.4% had an immediate postoperative improvement of the KPS. There was no influence of the histopathologic grade and of the location of the tumor along the SSS in the postoperative functional outcome. 5. Conclusions Recurrence of parasagittal meningiomas was predominant in males, in patients with grades II/III tumors, in patients who underwent subtotal resection, and in patients with more invasion of the SSS. Based on the rates of recurrence and on the mortality/morbidity, we concluded that total or subtotal resection without sinus resection was considered adequate for treating patients with parasagittal tumors. References [1] Adegbite AB, Khan MI, Paine KWE, Tan LK. The recurrence of intracranial meningiomas after surgical treatment. J Neurosurg 1983; 58:51 - 6. [2] Alvarez F, Roda JM, Romero MP, et al. Malignant and atypical meningiomas: a reappraisal of clinical, histological and computed tomographic features. Neurosurgery 1987;20:688. [3] Baird M, Gallagher PJ. Recurrent intracranial and spinal meningiomas: clinical and histological features. Clin Neuropathol 1989;8:41 - 4. [4] Bfker DK, Meurer H, Gullota F. Recurring intracranial meningiomas. Evaluation of some factors predisposing for tumor recurrence. J Neurosurg Sci 1985;29:11 - 7. [5] Bonnal J, Brotchi J. Surgery of the superior sagittal sinus in parasagittal meningiomas. J Neurosurg 1978;48:935 - 45. [6] Chan RC, Thompson GB. Morbidity, mortality, and quality of life following surgery for intracranial meningiomas: a retrospective study in 257 cases. J Neurosurg 1984;60:52 - 60. [7] Christensen D, Laursen H, Klinken L. Prediction of recurrence in meningiomas after surgical treatment. A quantitative approach. Acta Neuropathol, Suppl (Berl) 1983;61:130 - 4. [8] Cushing H, Eisenhardt L. Meningiomas: their classification, regional behavior, life history, and surgical end results. Springfield, Ill7 Charles C. Thomas; 1938. [9] Di Meco F, Li KW, Casali C, Ciceri E, Giombini S, Filippini G, Broggi G, Solero CI. Meningiomas invading the superior sagittal sinus: surgical experience in 108 cases. Neurosurgery 2004;55: 1263 - 72. [10] Giombini S, Solero CL, Lasio G, Morello G. Immediate and late outcome of operations for parasagittal meningiomas: report of 342 cases. Surg Neurol 1984;21:427 - 35.
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[11] Hakuba A. Reconstruction of dural sinus involved in meningiomas. In: Al-Mefty O, editor. Meningiomas. New York7 Raven Press; 1991. p. 371 - 82. [12] Hoessly GF, Olivecrona H. Report on 280 cases of verified parasagittal meningioma. J Neurosurg 1955;12:614 - 26. [13] J77skelanien J. Seemingly complete removal of histologically benign intracranial meningioma: late recurrence rate and factors predicting recurrence in 657 patients. A multivariate analysis. Surg Neurol 1986; 26:461 - 9. [14] Jellinger K, Slowik F. Histological subtypes and prognostic problems in meningiomas. J Neurol 1975;208:279 - 98. [15] Kallio M, Sankila R, Hakulinen T, J77skelanien J. Factors affecting operative and excess long-term mortality in 935 patients with intracranial meningiomas. Neurosurgery 1992;31:2 - 12. [16] Kleihues P, Cavenee WK, editors. Pathology and genetics of tumors of the nervous system. Lion7 IARC Press; 2000. p. 9 - 70. [17] Kujas M. Anatomo-pathologie. In: Phillipon J, editor. Les meningiomes re´cidivantsNeurochirurgie [Suppl], vol. 32. 1986. p. 15 - 24. [18] Logue V. Parasagittal meningiomas. Adv Tech Stand Neurosurg 1975;2:171 - 98. ¨ fner D, Hittmair A, Kitz A, Budka H. Classic, atypical, and [19] Maier H, O anaplastic meningiomas: three histopathological subtypes of clinical relevance. J Neurosurg 1992;77:616 - 23. [20] Mahmood A, Caccamo DV, Tomecek FJ, Malik GM. Atypical and malignant meningiomas: a clinicopathological review. Neurosurgery 1993;33:955 - 63. [21] Masuzawa H. Superior sagittal sinus plasty using falx flap in parasagittal meningioma. No Shinkei Geka 1977;5:707 - 13. [22] Philippon J, Cornu P. The recurrence of meningiomas. In: Al-Mefty O, editor. Meningiomas. New York7 Raven Press; 1991. p. 87 - 105. [23] Quest DO. Meningiomas: an update. Neurosurgery 1978;3:219 - 25. [24] Rohringer M, Sutherland GR, Louw DF, Sima AA. Incidence and clinicopathologic features of meningioma. J Neurosurg 1989;71: 665 - 72. [25] Sankila RK, Kallio M, J77skelainen J, Hakulinen T. Long-term survival of 1986 patients with intracranial meningioma diagnosed from 1953 to 1984 in Finland. Comparison of the observed and expected survival rates in population-based series. Cancer 1992; 70:1568 - 76. [26] Simpson D. The recurrence of intracranial meningiomas after surgical treatment. J Neurochem 1957;20:22 - 39. [27] Thomas HG, Dolman CL, Berry K. Malignant meningioma: clinical and pathological features. J Neurosurg 1981;55:929 - 34. [28] Wilkins RH. Parasagittal meningiomas. In: Al-Mefty O, editor. Meningiomas. New York7 Raven Press; 1991. p. 329 - 43. [29] Wilson CB. Meningiomas: genetics, malignancy, and the role of radiation in induction and treatment. The Richard C. Schneider Lecture. J Neurosurg 1994;81:666 - 75.
Commentary Surgery of parasagittal meningiomas is not always beasy.Q The nature, site, and extent of involvement of the dura and the bone are crucial factors that determine the course and conduct of surgery. Some of these tumors can be extensively vascular. The authors have treated 53 cases of parasagittal meningiomas over a period of 20 years. In 24 cases, they ligated the anterior third of the superior sagittal sinus without any clinical sequel. From their experience, the authors have found no significant difference was achieved in the outcome of patients undergoing radical (that included sacrifice of the sinus) or subtotal excision of the tumor.
Meningioma
Parasagittal meningiomas: follow-up review Benedicto Oscar Colli, MD, PhDa,4, Carlos Gilberto Carlotti Jr, MD, PhDa, Joa˜o Alberto Assirati Jr, MDa, Marcius Benigno Marques dos Santos, MDa, Luciano Neder, MD, PhDb, Antonio Carlos dos Santos, MD, PhDc a
Division of Neurosurgery, Department of Surgery, bDepartment of Pathology, and cDivision of Radiology, Hospital das Clinicas de Ribeira˜o Preto, Ribeira˜o Preto Medical School, University of Sa˜o Paulo, Ribeira˜o Preto, Sa˜o Paulo, Brazil Received 29 June 2006; accepted 2 August 2006
Abstract
Background: Parasagittal meningioma is one that fills the parasagittal angle, with no brain tissue between the tumor and the SSS. Invasion of the SSS is a challenge for complete removal and, consequently, for recurrence of these tumors. The objective of this study was to analyze the factors that influenced the clinical outcome of patients with parasagittal tumors surgically treated. Methods: Review of data on 53 patients with diagnosis of parasagittal meningiomas surgically treated from 1984 to 2004. Thirty-four (64.2%) were female and 19 (35.8%) were male; age ranged from 18 to 81 years old (mean, 54.98 F 5.80). Follow-up ranged from 2 to 261 months (mean, 93.71 F 68.45). The patients were operated on using microsurgical techniques. Tumors in the anterior third (9) or occluding the SSS (5) were removed with the sinus; tumors touching/pouching the SSS (20) were removed and its dural attachment coagulated; tumors invading one sinus wall (10) were removed with partial excision and reconstruction of the sinus wall, and tumors invading more than one sinus wall in the posterior two thirds of the SSS (7) had a subtotal removal. No attempt at sinus resection and reconstruction was performed for tumors placed in the posterior two thirds of the SSS. Analysis of the patient outcome was done using survival and RFS Kaplan-Meier curves. The v 2, Fisher exact, log-rank, Mann-Whitney, and Kruskall-Wallis ANOVA tests were used for comparing demographic data, survival curves, proportions, and medians, respectively. Results: Total and subtotal resection were achieved in 85% and 13.1%, respectively. Males had better survival than females ( P = .0252). Total RF rates were 10%, 25%, and 100% at 5 years and 100%, 50%, and 100% at 10 years for patients with meningiomas WHO grades I, II, and III, respectively. The RF survival curve was better for patients with grade I meningioma (grades I vs II vs III, P = .0001). There was no difference between the RF survival curves according to age, histopathologic WHO grade, location along or invasion of the SSS, and extent of resection. Males ( P = .0401), WHO grade I ( P b .0001), total resection ( P = .0139), and less sinus invasion ( P = .0308) had better RFS curves. Operative, surgery-related, and overall mortality were 1.9%, 5.4%, and 26.4%, respectively. Conclusions: Recurrence of parasagittal meningiomas predominated in males, in grades II/III tumors, after subtotal resection, and with more invasion of the SSS. Subtotal or total resections without sinus resection were considered adequate for treating these patients. D 2006 Elsevier Inc. All rights reserved.
Keywords:
Parasagittal meningiomas; Surgical treatment; Survival curves; Recurrence-free survival curves; Extension of resection
Abbreviations: ANOVA, analysis of variance; CT, computed tomography; KPS, Karnofsky Performance Scale; MR, magnetic resonance; RFS, recurrence free survival; SSS, superior sagittal sinus; WHO, World Health Organization. 4 Corresponding author. Departamento de Cirurgia, HCFMRP, Campus Universita´rio, USP, 14048-900 Ribeira˜o Preto, SP, Brazil. Tel.: +55 3602 2498; fax: +55 3602 2498. E-mail address: [email protected] (B.O. Colli). 0090-3019/$ – see front matter D 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.surneu.2006.08.023
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Table 2 Initial signs and symptoms in 51 patients with parasagittal meningiomas
1. Introduction Cushing and Eisenhardt [8] defined parasagittal meningioma as one that fills the parasagittal angle, with no brain tissue between the tumor and the SSS. Parasagittal meningiomas comprise 21% to 31% of intracranial meningiomas [6,8,13,15,28,29], and the distribution of the meningiomas along the SSS ranged from 14.8% to 33.9% in the anterior third, from 44.8% to 70.4% in the middle third, and from 9.2% to 29.6% in the posterior third of the sinus [8 -10,12]. Most parasagittal meningiomas are benign tumors that can be cured with surgical treatment. Nevertheless, despite the improvement in the diagnosis and topographic evaluation by CT scans and MR imaging, the involvement of the SSS and surrounding veins, specially for tumors located in the middle third of the SSS, may preclude their complete removal, making the management of these tumors a real challenge because of the relatively high mortality and morbidity [5,9,28]. The routine use of microsurgical techniques has reduced the surgical mortality, but the postoperative morbidity and rate of recurrence for these tumors remain high [9]. The objective of this study was to analyze factors that influenced the clinical outcome of a group of patients with parasagittal meningiomas treated at the Division of Neurosurgery of the Hospital das Clı´nicas, Ribeira˜o Preto Medical School, University of Sa˜o Paulo. 2. Clinical material and methods 2.1. Patient population Parasagittal meningioma cases comprised 19.24% (61) of 317 patients with a radiologic diagnosis of intracranial meningioma assisted from 1984 to 2004. The design of this study was a retrospective review of data on 53 consecutive patients with parasagittal meningiomas submitted to surgical treatment. Diagnosis of these tumors was performed using CT and/or MR imaging of the skull. Eight patients with radiologic diagnosis were conservatively treated (small and calcified tumors in aged patients or refused surgical treatment). According to the histopathologic WHO classification [16], 41 patients presented benign grade I meningiomas (16 transitional, 15 meningothelial, 4 psammomatous, Table 1 Summary of demographic data in 53 patients with parasagittal meningiomas Characteristic
Sex Female Male Female/male Age (y)4 Age range (y) Female Male
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Meningiomas
Total
Grade I
Grade II
Grade III
29 12 2.42:1 56.44 F 16.12
4 4 1:1 52.38 F 16.61
1 3 1:3 45.3 F 9.84
34 19 1.79:1 54.98 F 15.89
24-78 18-81
34-70 27-67
34 45-58
24-78 18-81
4 Values are presented as the mean F SD.
Signs and symptoms Generalized seizures Partial seizures Headache Hemiparesis Incidental Visual loss Behavior disturbance Monoparesis Disorientation Other 4
Location along the superior sagittal sinus Anterior third
Middle third
Posterior third
9 – 7 3 2 2 2
8 2 3 4 3 1 1 2 2 1
2 – – 1 1 1 – – – 1
1
4 These signs and symptoms included apathy, drowsiness, dementia, depression, monoparesis, dysphasia, loss of initiative, and tremor in 1 patient with meningioma of the anterior third, and irritability, dysphasia, diplopia, agitation, urinary incontinence, dysphasia, hemianopsia, and ataxia in 1 patient with meningioma of the middle third of the superior sagittal sinus.
2 angiomatous, 3 fibroblastic, 1 secretory), 8 had grade II (6 atypical, 2 grade II hemangiopericytomas), and 4 grade III meningiomas. The hemangiopericytomas were included because they were not diagnosed previously and because they pose the same technical problems during surgery. 2.2. Clinical findings The most important demographic characteristics of patients are presented in Table 1. There was a female predominance in all patients (average female/male ratio of 1.8:1) and in patients with grade I meningiomas. The sex distribution was similar for patients with grade II meningiomas, and, despite the small number, there was a male predominance in patients with grade III meningiomas. Age ranged from 18 to 81 years old (mean, 54.98 F 15.89). There was no difference between the mean age of patients in Table 3 Signs and symptoms presented at the diagnosis in 51 patients with parasagittal meningiomas Signs and symptoms Generalized seizures Partial seizures Headache Hemiparesis Incidental Visual loss Behavior disturbance Aphasia/dysphasia Monoparesis Disorientation Other 4
Location along the superior sagittal sinus Anterior third
Middle third
Posterior third
9 – 7 4 3 3 2 1 1 1
10 2 6 4 3 1 1 4 3 2 1
2 – – 1 1 1 – – – 1
4 These signs and symptoms included apathy, ataxia, dizziness, pyramidal signs, drowsiness, dementia, depression, loss of initiative, tremor, coma, and hemiparesis in 1 patient with meningioma of the anterior third; irritability, diplopia, agitation, urinary incontinence, hemianopsia, pyramidal signs, mental confusion, ataxia, and difficulty in walking in 1 patient with meningioma of the middle third; and ataxia and dizziness in 1 patient with meningioma of the posterior third of the superior sagittal sinus.
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2.4. Functional outcome
Fig. 1. Survival curve for patients with parasagittal meningiomas according to sex. Significant difference ( P = .0252, df = 1 [log-rank test]).
relation to the histopathologic type of tumor and considering grades I vs II and III ( P = .5413, 5 groups [Kruskall-Wallis nonparametric ANOVA]). The clinical signs and symptoms at onset and at diagnosis, according to the location along the SSS, and the average duration of symptoms are summarized in Tables 2 and 3. Follow-up ranged from 2 to 261 months (mean, 93.71 F 68.45; median, 78.0). Twenty-four (45.3%) were placed in the anterior third of the SSS, 26 (49.1%) in the middle, and 3 (5.6%) in the posterior third of the sinus. 2.3. Management of the disease 2.3.1. Surgical treatment The patients were operated on using microsurgical techniques and special attention was given to the preoperative evaluation of the permeability of the SSS and of the location of parietal veins using digital angiography and, more recently, MR imaging angiography. Nine patients (6 grade II, 3 grade III meningiomas) underwent adjuvant conventional radiotherapy. No attempt at complete sinus resection followed by reconstruction was performed when the tumor was placed in the posterior two thirds of the SSS. The extent of resection was assessed macroscopically during surgery and postoperatively using CT or MR imaging 48 hours and 6 months after operation (radical removal when there was no evidence or doubt about residual tumor in the MR image; subtotal when the resection was N 90%; and partial when the resection was b 90%). Forty-five (85%) patients had radical tumor resection, 7 (13.1%) had subtotal resection, and 1 (1.9%) had partial resection but died during surgery. The follow-up median for patients who underwent radical or subtotal resection was not significantly different ( P = .3287, Mann-Whitney U test). All patients with WHO grades II and III meningiomas had initial total resection. Based on intraoperative findings, invasion of the SSS could be classified [5] in 37 (69.8%) patients with tumors types I to IV (sinus permeable) and in 16 (30.2%) with types V to VIII (sinus almost/completely occluded).
Because of the small number of patients with grades II and III tumors and with tumors in the posterior third of SSS, analysis of outcome was performed comparing patients with tumors in the anterior vs middle third and patients with histopathologic grades I vs II to III meningiomas. The preoperative, postoperative (first 10 days), and follow-up outcome were analyzed using the KPS to measure the degree of disability. Patients were classified into 1 of 3 groups. (1) Those with normal function or minimal symptoms and can work (KPS score, 80-100); (2) those who are independent but cannot work (KPS score, V 70); and (3) those with moderate or severe disability (KPS score, V 50). For patients who experienced tumor recurrence and consequent clinical deterioration, the best KPS score obtained during the follow-up course was used. For patients who died during the immediate postoperative course, the KPS score acquired before death was used to indicate both the immediate postoperative and follow-up scores. Three patients did not attend 6 months of follow-up and did not receive a KPS score at this time. Follow-up analysis was performed using the KaplanMeier survival and RFS curves and rates in relation to sex, age, histopathologic grade, location of tumor, extent of resection, and invasion of SSS. Nine patients with tumors in the anterior third and 5 patients with the middle/posterior third of the SSS occluded by the tumor were excluded from the last analysis because the sinus was removed en bloc with the tumor. 2.5. Statistical analysis Statistical analysis was performed using the v 2 and the Fisher exact tests for comparing proportions; the MannWhitney U test and the Kruskall-Wallis nonparametric ANOVA for comparison of medians; and the log-rank test for comparison of survival curves and rates. An a error probability not exceeding 5% was considered significant for 2-tailed probability tests. The tests were performed using
Fig. 2. Recurrence-free survival curve for all patients with parasagittal meningiomas according to sex. Significant difference ( P = .0401, df = 1 [log-rank test]).
B.O. Colli et al. / Surgical Neurology 66 (2006) S3:20–S3:28
Fig. 3. Recurrence-free survival curves for patients with parasagittal meningiomas according to the WHO histopathologic grades. Significant difference ( P b .0001, df = 2 [log-rank test]).
GraphPad PRISM (version 3.0; GraphPad Software, Inc, San Diego, CA, USA).
3. Results 3.1. Follow-up review 3.1.1. Survival Fig. 1 presents the survival curves for all patients according to sex. The 5-year survival estimates were 93.7% and 79.3%, and the 10-year survival estimates were 79.8% and 35.3% for female and male patients, respectively. The survival curve was better for females ( P = .0252, df = 1 [log-rank test]). There was no significant difference (log-rank test) for the survival curves according to sex for patients with grade I meningiomas ( P b .2291, df = 1); according to histopathologic grades I, II, and III ( P = .4557, df = 2) and subtypes of grade I ( P b .3751, df = 3), according to the location along the SSS (anterior vs posterior two thirds) for all patients ( P b .5204, df = 1) and for patients with grade I meningiomas ( P b .1544, df = 1); and according to the invasion of the SSS (grades I-IV vs grades V-VIII [5]) for all patients ( P b .4197 [log-rank test]) and for patients with WHO grade I meningiomas ( P b .4737 [log-rank test]). 3.1.2. Recurrence-free survival Total recurrence rate at follow-up was 32.7% (17 patients), distributed in 17.5% (7 patients), 75% (6 patients), and 100% (4 patients) of patients with WHO grades I, II, and III meningiomas, respectively. There was significant difference (Fisher exact test) between the rates for patients with WHO grades I and II ( P = .0033, df = 1), and between grades I and III ( P = .0027, df = 1), and no significant difference between grades II and III ( P = .5152, df = 1). The RF rates were 80.8%, 71.4%, and 0% at 5 years, and 67.5%, 17.9%, and 0% at 10 years for patients with grades I, II, and III meningiomas, respectively. Total RF rates were
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27.6% at 5 years and 47% at 10 years. Recurrences for all patients occurred in the first 5 years in 10 patients (58.8), after 5 years in 7 (41.2%), and after 10 years in 2 (11.8%) (at 127 [atypical meningioma] and 144 [hemangiopericytoma] months). Among patients with WHO grade I meningiomas, recurrence occurred in 4 (57.1%) patients in the first 5 years and in 3 (42.9%) between 5 and 10 years. Fig. 2 presents the RFS curves for all patients according to sex. The 5-year RF estimates were 83.7% and 63.2%, and the 10-year survival estimates were 69.8% and 14.7% for female and male patients, respectively. Recurrence-free survival curve was better for females than for males for all patients ( P = .0401, df = 1 [log-rank test]). There was no significant difference (log-rank test) for the RFS curves according to sex for patients with grade I meningiomas ( P b .1209, df = 1) and according to age (10-29 vs 30-39 vs 40-49 vs 50-59 vs 60-69 vs 70-90 years old, P b .3344, df = 4 [log-rank test] and 10-49 vs 50-90 years old, P b .2800, df = 1) for all patients. The RFS curves according to histopathologic classification are presented in Fig. 3. The 5-year RFS estimates were 80.8%, 67.5%, and 0%, and the 10-year survival estimates were 67.5%, 11.4%, and 0% for patients with grades I, II, and III meningiomas, respectively. The RFS curve was better for grade I than for grades II and III ( P b .0001, df = 2 [log-rank test] and P b .0001, df = 1 [log-rank test for trend]). The medians of the RFS curves were also different ( P = 0001, df = 2 [Kruskall-Wallis–ANOVA]). They were significant (Dunn multiple comparisons posttest) for grades I and II ( P b .05), and for grades I and III, and not significant for grades II and III ( P N .05). Patients with grade I tumors had less recurrence than those with grades II and III tumors. The RFS curves for patients with grade I tumors were not significantly different ( P b .3537, df = 3 [log-rank test]) according to their histopathologic subtypes. The RFS curves for all patients and for patients with grade I tumors according to the extent of resection (radical vs subtotal) are depicted in Figs. 4 and 5. Radical resection allowed better RFS curve (log-rank test) than subtotal for all
Fig. 4. Recurrence-free survival curves for all patients with parasagittal meningiomas according to the extension of resection. Significant difference ( P b .0139, df = 1 [log-rank test]).
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Fig. 5. Recurrence-free survival curves for patients with WHO grade I parasagittal meningiomas according to the extent of resection. Significant difference ( P = .0305, df = 1 [log-rank test]).
patients ( P b .0139, df = 1) and for patients with grade I meningiomas ( P = .0305, df = 1). Fig. 6 presents the RFS curves for all patients according to the location along the SSS (anterior vs middle/posterior third). The RFS curve was better (log-rank test) for patients with tumor in the anterior third of the SSS ( P b .0112, df = 1), but it was similar for patients with grade I meningiomas ( P b .1544, df = 1 [log-rank test]). The RFS curves for all patients and for patients with WHO grade I meningiomas in relation to the extension of invasion of the SSS (Bonnal and Brotchi grades I-IV vs V-VIII) are depicted in Figs. 7 and 8, respectively. The curves were better (log-rank test) for less invasion of the SSS for all patients ( P b .0308, df = 1 [log-rank test]) and for patients with grade I meningiomas ( P b .0301, df = 1).
Fig. 7. Recurrence-free survival curves for all patients with parasagittal meningiomas according to the invasion of superior sagittal sinus [5]. Significant difference ( P b .0308, df = 1 [log-rank test]).
One patient with type 2 neurofibromatosis and multiple meningiomas (grade I) died during her seventh surgery after circulatory shock due to massive hemorrhage. Two patients (grades I and II) died 2 months after surgery because of
postoperative complications (pulmonary infection and pulmonary embolism after deep venous thrombosis), and 11 patients died during the follow-up period (operative mortality, 1.9%; surgery-related mortality, 5.7%; and overall mortality, 26.4%). During the follow-up, 3 deaths were due to progression of grade III meningiomas and 8 deaths were not related to the tumor (6 grade I tumors, 1 grade II, 1 grade III). The age of these patients ranged from 65 to 88 years old (65, 70, 73, 77, 82, 85, and 88; mean, 77.14; SD, F8.355). Two patients (grade I) developed postoperative monoparesis, 1 patient (grade II) developed tetraparesis, and 1 (grade I) developed crural paraparesis, totaling 4 (7.8%), 1 permanent and 3 transient, all of them located in the middle third of the SSS. Two patients (3.9%) developed osteomyelitis treated with removal of the flap and later cranioplasty, 4 (3.9%) had a subgaleal collection treated with aspiration, and 1 (1.9%) had a fluid collection over a bovine pericardial graft, detected on a control CT; this collection was conservatively treated and became calcified. Nonneurologic complications observed were venous thrombosis in 2 (3.9%)
Fig. 6. Recurrence-free survival curves for patients with parasagittal meningiomas according to the location along the superior sagittal sinus. Significant difference ( P b .0112, df = 1 [log-rank test]).
Fig. 8. Recurrence-free survival curves for patients with WHO grade I parasagittal meningiomas according to the invasion of the superior sagittal sinus [5]. Significant difference ( P b .0301, df = 1 [log-rank test]).
3.2. Mortality and morbidity
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Table 4 Preoperative, postoperative, and follow-up functional status Functional status
KPS score Preoperative
Immediate postoperative
Follow-up
WHO histopathologic grade Grade I No. of patients Normal or minimal 80-100 symptoms and working Independent, 70 not working Moderate or 50 severe disability
Grades II/III Total
41 12 30 (56.6%) 5 (9.4%)
9 (17%) 2 (3.8 %)
7 (1.3.2%) –
53 35 (66%)
Grade I
Grades II/III Total
40 12 35 (57.7%) 5 (9.6 %)
Grade I
Grades II/III Total
52 39 11 40 (76.9 %) 33 (66%) 5 (10%)
50 38 (76%)
16 (30.2%)
4 (7.7 %)
5 (9.6%)
9 (17.3%)
3 (6%)
4 (8%)
7 (14%)
2 (3.8%)
1 (1.9 %)
2 (3.8%)
3 (5.8%)
3 (6%)
2 (4%)
5 (10%)
patients (1 followed by fatal pulmonary embolism) and fatal pulmonary infection in 1 (1.9%) patient. 3.3. Postoperative functional outcome Preoperative, immediate postoperative, and follow-up functional disabilities assessed by KPS are presented in Table 4. The scores were similar (v 2 test, df = 2) in all evaluations ( P = .3274 for all patients, P = .2110 for patients with grade I tumors, and P = .9781 for patients with grades II-III tumors). Preoperatively, 18 (34%) patients had KPS scores of 70 or less, and, postoperatively, 12 (23.1%) had scores of at least 70 (no significant difference, P = .2809, Fisher exact test, df = 1). Four (7.7%) patients experienced deterioration postoperatively (KPS, V 70) and 7 (13.4%) experienced improvement (KPS, z 80). Assessment at 6 months demonstrated 1 additional patient (grade I) with KPS score of 70 or less. 4. Discussion
the sinus (primarily or with a graft). Tumor invading only the external layer of the lateral sinus wall can be completely resected by laminating the external layer of the tumor and preserving the internal layer of the sinus wall. Primary closure of the SSS can be accomplished for tumor invading the lateral angle of the sinus. The piece of tumor attached to the sinus can be resected followed by a progressive running suture along the sinus wall. During this resection, blood flow should be interrupted with vascular clamps, forceps, or with finger compression to prevent air embolism. When some perforations occurred in the sinus wall during resection, we used a flap from the falx [21], rotated upward, and sutured anteriorly, posteriorly, and superiorly to reconstruct the lateral wall of the sinus. Resection and reconstruction of the sinus are feasible, but they may be followed by significant morbidity [5,11]. In our series, we opted to perform a subtotal resection when the posterior two thirds of the sinus was significantly invaded by a tumor and we never interrupted and reconstructed the sinus.
4.1. Surgical treatment
4.2. Survival
The treatment of parasagittal meningiomas is predominantly surgical. Besides major hemorrhage from the scalp, bone, dura, tumor, and sinus, the attachment to the dura, sinus, or falx makes it more difficult to remove the tumor and increases the chance of injury to the normal brain. Invasion of the sinus is a major problem in the resection of these tumors. It is a general concept that the anterior third of the SSS may be resected without sequelae [5,23], but resection of the posterior two thirds of the sinus may cause severe, permanent damage to the adjacent brain if the sinus is patent. We observed no morbidity or mortality that could be attributed to ligature of the anterior third of the SSS in 24 patients, which corroborates this concept. When the sinus is completely occluded, it may be resected without significant risks [5,9,23]. The surgeon has 3 options when the SSS is invaded: (1) leave a small portion of the tumor attached to the sinus and wait for the occlusion of the sinus by the tumor and for the development of collateral venous drainage to try a late complete resection; (2) resect the tumor to obliterate the sinus; or (3) resect and reconstruct the involved part of
Sex was the only significant variable for survival among patients with parasagittal meningiomas (better survival curve for females in relation to males). Other factors such as age, WHO histopathologic grades (grades I vs II vs III), the extent of resection (Simpson grades I/II vs grade IV; radical vs subtotal), location of the tumors along the SSS (anterior third vs middle and posterior third), and the extent of compromising of the SSS according to Bonnal and Brotchi [5] grades (I-IV vs V-VIII) for all patients and for patients with grade I parasagittal meningiomas were not significant for survival. 4.3. Recurrence Recurrence of parasagittal meningiomas occurs in 7.9% to 29% [3,6,9,13,22,26], and it is dependent on the extent of the follow-up (5%-17.7% at 5 years and in 14.4%-24% at 10 years) [6,9,10,22]. Recurrence rate in all the follow-up in our series was 32.7%, and it was 12% at 5 years and 16% at 10 years. Most authors agree that recurrence rates for patients with atypical or malignant meningiomas are greater than for patients with WHO grade I [1,2,13,19,20,24,27],
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and this is also true for patients with parasagittal meningiomas as demonstrated by Di Meco et al [9] and by our results. There was no patient with grade III tumor without recurrence at the 5-year follow-up. Among the subtypes of WHO grade I intracranial meningiomas, psammomatous tumors with a high density of calcification rarely recur [17], and the angioblastic meningiomas, even if they are separated from the hemangiopericytomas, seem to have a markedly high rate of recurrence [3,7,14]. Despite no significant difference among the histopathologic subtypes of WHO grade I tumors in our series, there was no recurrence among patients with psammomatous tumors. Delay in recurrence is variable among patients with intracranial meningiomas and it has been detected early after the routine use of follow-up CT scans [6]. Recurrence has been reported as more than half occurring by the end of the fourth/fifth year [22], and our results agree with these findings. Late (after 10 years) recurrence in our series (11.8% of the recurrences) was similar to that reported by others [22], but, interestingly, these recurrences occurred in patients with an atypical meningioma and a hemangiopericytoma. Many factors are reputed to influence the recurrence of all intracranial meningiomas. For some of them, this role is incontestable, but for others it is controversial. Regarding age and sex, some authors related that the risk is increased and the delay of recurrence is shorter in younger patients and that there is no difference in the recurrence between sexes for patients with any kind of intracranial meningiomas [4,22] and parasagittal meningiomas [9]. Simpson, in 1957 [26], established the recurrence of meningiomas according to the extent of resection, and since then other authors have confirmed his findings [6,9,13]. Recurrence at 5 years after tumor plus dural resections ranges from 5% to 16%, after total tumor resection from 11.9% to 18%, and after partial resection of the tumor from 14% to 41.9% [9,10]. Di Meco et al [9] reported no interference of tumor location along the SSS. In our series, age did not interfere with the recurrence rates. Females had less recurrence than males for all patients. The extent of resection influenced the decrease in recurrence rates for all patients with parasagittal meningiomas and for patients with WHO grade I meningiomas. Considering all patients, patients with tumors located in the anterior third of the SSS had significantly less recurrence than patients with tumors located in the middle and posterior third of the SSS, but there was no difference for patients with the subtypes of WHO grade I meningiomas. The extent of invasion of the SSS (Bonnal and Brotchi grades I-IV vs grades V-VIII) influenced positively the rates of recurrence for all patients and for patients with WHO grade I meningiomas. Despite a high recurrence rate in all the follow-up (32.7%), and the better RFS curves for radical resection in our series, if we consider that the recurrent rates were 12% at 5 years and 16% at 10 years and that more than half of the recurrences occurred in patients with WHO grades II and III tumors, we can consider that our results justify our less aggressive policy in relation to the resection of the SSS.
4.4. Mortality and morbidity Operative mortality for resection of parasagittal meningiomas varied from 1.85% to 12.3% [6,8,9,10,12,18]. Mortality is associated significantly with old age [25], is greater for patients with tumor located in the middle third of the sinus, and did not depend on the extension of the resection [9,10]. Di Meco et al [9] reported a decrease from 3.7% to 1.85% in operative mortality after the introduction of microsurgical techniques in the treatment of patients with parasagittal meningiomas operated on from 1986 to 2001. Causes of death among the patients of Giombini et al [10] were predominantly cerebral swelling, followed by pulmonary embolism, postoperative hematoma, cardiac failure, and bronchopneumonia. Predominance of cerebral swelling in patients with tumor in the middle third of the SSS probably indicates surgical damage to cortical veins closely related to the tumor. The operative mortality (first 30 days after surgery) observed in our series was 1.9%, the surgeryrelated mortality was 5.7%, and the overall mortality rate in the follow-up was 26.4%. Surgery-related deaths were caused by circulatory chock in 1 patient, by pulmonary infection in another, and by pulmonary embolism in a third patient. In the follow-up, 8 deaths were not related to tumor and 3 patients with grade III meningiomas died because of progression of the disease. Morbidity after resection of parasagittal meningiomas remains significant. Transient neurologic worsening in the immediate postoperative period was common (8.3%) among the patients of Di Meco et al [9] and was related to the great size of the tumor and to the location in the middle and posterior third of the SSS. The authors speculate that this impairment was caused by transitory venous engorgement and difficulties in venous drainage caused by sinus stenosis in the event of marginal resection. Neurologic recovery probably was favored by rearrangement of venous anastomosis and by opening of alternative venous outflow pathways that ultimately could restore the conditions of normal venous drainage. Other operative complications observed by the authors were intracranial hematomas (2 patients, 1.8%), subgaleal fluid collection in 11 (10%) patients (3 resolved spontaneously, 6 required lumbar puncture, and 3 required surgical treatment), wound infection requiring surgical treatment in 3 (2.7%), and new onset of seizures in 3 patients (7.7%). Nonneurologic complications included 3 (2.7%) deep venous thrombosis. We observed neurologic deterioration in 4 (7.8%) patients and it was permanent in one of them. All neurologic deterioration occurred in patients with tumors located in the middle third of the SSS. As these complications are generally caused by interruption of the SSS or by lesion of cortical veins draining to the SSS, every effort should be exerted to preserve the bridging veins located over or anterior or posterior to the tumor to avoid surgical interruption or inducing thrombosis of such veins which could lead to regional venous infarction with delayed neurologic deficit. Other complications observed were
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subgaleal collection, wound infection, and epidural collection. Systemic complications observed include venous thrombosis in 3.9%, which was responsible for the death of 1 patient. 4.5. Postoperative functional outcome As postoperative neurologic worsening is not uncommon, functional outcome sometimes may worsen after surgical treatment of parasagittal meningiomas. Di Meco et al [9] reported an immediate postoperative worsening of preexisting condition in 11.1% of cases and most of them improved sometime later, after the improvement of the neurologic deficit. In our series, 7.7% of patients had a worse immediate postoperative KPS than preoperatively, but 13.4% had an immediate postoperative improvement of the KPS. There was no influence of the histopathologic grade and of the location of the tumor along the SSS in the postoperative functional outcome. 5. Conclusions Recurrence of parasagittal meningiomas was predominant in males, in patients with grades II/III tumors, in patients who underwent subtotal resection, and in patients with more invasion of the SSS. Based on the rates of recurrence and on the mortality/morbidity, we concluded that total or subtotal resection without sinus resection was considered adequate for treating patients with parasagittal tumors. References [1] Adegbite AB, Khan MI, Paine KWE, Tan LK. The recurrence of intracranial meningiomas after surgical treatment. J Neurosurg 1983; 58:51 - 6. [2] Alvarez F, Roda JM, Romero MP, et al. Malignant and atypical meningiomas: a reappraisal of clinical, histological and computed tomographic features. Neurosurgery 1987;20:688. [3] Baird M, Gallagher PJ. Recurrent intracranial and spinal meningiomas: clinical and histological features. Clin Neuropathol 1989;8:41 - 4. [4] Bfker DK, Meurer H, Gullota F. Recurring intracranial meningiomas. Evaluation of some factors predisposing for tumor recurrence. J Neurosurg Sci 1985;29:11 - 7. [5] Bonnal J, Brotchi J. Surgery of the superior sagittal sinus in parasagittal meningiomas. J Neurosurg 1978;48:935 - 45. [6] Chan RC, Thompson GB. Morbidity, mortality, and quality of life following surgery for intracranial meningiomas: a retrospective study in 257 cases. J Neurosurg 1984;60:52 - 60. [7] Christensen D, Laursen H, Klinken L. Prediction of recurrence in meningiomas after surgical treatment. A quantitative approach. Acta Neuropathol, Suppl (Berl) 1983;61:130 - 4. [8] Cushing H, Eisenhardt L. Meningiomas: their classification, regional behavior, life history, and surgical end results. Springfield, Ill7 Charles C. Thomas; 1938. [9] Di Meco F, Li KW, Casali C, Ciceri E, Giombini S, Filippini G, Broggi G, Solero CI. Meningiomas invading the superior sagittal sinus: surgical experience in 108 cases. Neurosurgery 2004;55: 1263 - 72. [10] Giombini S, Solero CL, Lasio G, Morello G. Immediate and late outcome of operations for parasagittal meningiomas: report of 342 cases. Surg Neurol 1984;21:427 - 35.
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[11] Hakuba A. Reconstruction of dural sinus involved in meningiomas. In: Al-Mefty O, editor. Meningiomas. New York7 Raven Press; 1991. p. 371 - 82. [12] Hoessly GF, Olivecrona H. Report on 280 cases of verified parasagittal meningioma. J Neurosurg 1955;12:614 - 26. [13] J77skelanien J. Seemingly complete removal of histologically benign intracranial meningioma: late recurrence rate and factors predicting recurrence in 657 patients. A multivariate analysis. Surg Neurol 1986; 26:461 - 9. [14] Jellinger K, Slowik F. Histological subtypes and prognostic problems in meningiomas. J Neurol 1975;208:279 - 98. [15] Kallio M, Sankila R, Hakulinen T, J77skelanien J. Factors affecting operative and excess long-term mortality in 935 patients with intracranial meningiomas. Neurosurgery 1992;31:2 - 12. [16] Kleihues P, Cavenee WK, editors. Pathology and genetics of tumors of the nervous system. Lion7 IARC Press; 2000. p. 9 - 70. [17] Kujas M. Anatomo-pathologie. In: Phillipon J, editor. Les meningiomes re´cidivantsNeurochirurgie [Suppl], vol. 32. 1986. p. 15 - 24. [18] Logue V. Parasagittal meningiomas. Adv Tech Stand Neurosurg 1975;2:171 - 98. ¨ fner D, Hittmair A, Kitz A, Budka H. Classic, atypical, and [19] Maier H, O anaplastic meningiomas: three histopathological subtypes of clinical relevance. J Neurosurg 1992;77:616 - 23. [20] Mahmood A, Caccamo DV, Tomecek FJ, Malik GM. Atypical and malignant meningiomas: a clinicopathological review. Neurosurgery 1993;33:955 - 63. [21] Masuzawa H. Superior sagittal sinus plasty using falx flap in parasagittal meningioma. No Shinkei Geka 1977;5:707 - 13. [22] Philippon J, Cornu P. The recurrence of meningiomas. In: Al-Mefty O, editor. Meningiomas. New York7 Raven Press; 1991. p. 87 - 105. [23] Quest DO. Meningiomas: an update. Neurosurgery 1978;3:219 - 25. [24] Rohringer M, Sutherland GR, Louw DF, Sima AA. Incidence and clinicopathologic features of meningioma. J Neurosurg 1989;71: 665 - 72. [25] Sankila RK, Kallio M, J77skelainen J, Hakulinen T. Long-term survival of 1986 patients with intracranial meningioma diagnosed from 1953 to 1984 in Finland. Comparison of the observed and expected survival rates in population-based series. Cancer 1992; 70:1568 - 76. [26] Simpson D. The recurrence of intracranial meningiomas after surgical treatment. J Neurochem 1957;20:22 - 39. [27] Thomas HG, Dolman CL, Berry K. Malignant meningioma: clinical and pathological features. J Neurosurg 1981;55:929 - 34. [28] Wilkins RH. Parasagittal meningiomas. In: Al-Mefty O, editor. Meningiomas. New York7 Raven Press; 1991. p. 329 - 43. [29] Wilson CB. Meningiomas: genetics, malignancy, and the role of radiation in induction and treatment. The Richard C. Schneider Lecture. J Neurosurg 1994;81:666 - 75.
Commentary Surgery of parasagittal meningiomas is not always beasy.Q The nature, site, and extent of involvement of the dura and the bone are crucial factors that determine the course and conduct of surgery. Some of these tumors can be extensively vascular. The authors have treated 53 cases of parasagittal meningiomas over a period of 20 years. In 24 cases, they ligated the anterior third of the superior sagittal sinus without any clinical sequel. From their experience, the authors have found no significant difference was achieved in the outcome of patients undergoing radical (that included sacrifice of the sinus) or subtotal excision of the tumor.