Journal of Clinical Neuroscience (2004) 11(8), 863–867 0967-5868/$ - see front matter ª 2004 Elsevier Ltd. All rights reserved. doi:10.1016/j.jocn.2004.02.007
Clinical study
Experience of a single institution treating foramen magnum meningiomas M. Necmettin Pamir
MD,
€ rker Kılıc Tu
MD PHD,
€ Koray Ozduman
MD,
ur Tu € re MD Ug
Department of Neurosurgery, Faculty of Medicine, Marmara University, Istanbul, Turkey
Available online Summary Despite the introduction of skull base approaches, there is still controversy in the optimum surgical management of foramen magnum meningiomas. Between January 1990 and January 2003, 22 patients underwent 23 surgical procedures with a diagnosis of foramen magnum meningioma at Marmara University, Department of Neurosurgery. The suboccipital approach was used for 2 posteriorly located tumors with radiological total removal. The paramedian suboccipital approach was replaced by the far-lateral modification in the treatment of ventral meningiomas. 1 of the 20 ventral tumors was operated twice. The classical suboccipital approach was followed by the far-lateral modification. A gross-total removal was achieved in 21 patients. The overall morbidity was 32%. No specific and clinically significant complications attributable to the far-lateral modification were observed. The far-lateral approach has improved the success of surgery in ventrally located lesions. The posterior suboccipital approach is still indicated in the removal of lesions placed posterior to the dentate ligament. ª 2004 Elsevier Ltd. All rights reserved. Keywords: foramen magnum, meningioma, far-lateral approach, skull base surgery
INTRODUCTION Foramen magnum meningiomas are rare and comprise 0.3–3.2% of all meningiomas.5 It is the most common neoplastic lesion arising at the craniocervical junction.3–5;13;17;18;20;22;25;39;40 These lesions arise between the lower 1/3 clivus and the C1–C2 area. A detailed description on the boundaries of the region is provided by George et al.18 A classification scheme exists according to the localization of the dural attachment.17 Due to their complex anatomy and invasion of vital structures, ventral and ventro-lateral meningiomas pose the most complex surgical problems to the treating surgeon. Controversy still exists about the optimal mode of treatment4;5;10;19;27;28;31 and the optimal surgical approach.4;5;10;19;31;37 Two surgical approaches are routinely used to treat foramen magnum meningiomas: the far-lateral transcondylar approach and the inferior suboccipital approach with modifications. Skull base approaches, mainly the use of the far-lateral approach, have considerably increased the success rate in the surgical removal of foramen magnum meningiomas. Retrospective analysis of the presented series elucidates the significant contribution of the transcondylar approach to the surgical management of this challenging disease in terms of extent of resection. Patients and methods Between January 1990 and January 2003, twenty two patients underwent surgical treatment for foramen magnum meningiomas at Marmara University Hospital and Marmara University Institute for Neurosurgical Sciences. All patients had contrast enhanced MRI examinations preoperatively. 3D-CT, CT angiography and conventional angiography were also used if necessary to modify surgical technique. Extent Received 28 December 2003 Accepted 23 February 2004 Correspondence to: Necmettin Pamir MD, Department of Neurosurgery, Marmara University, Tophanelioglu caddesi, No: 13/15 Altunizade, Istanbul 81190, Turkey. Tel.: +90-533-767-33-65; Fax: +90-216-305-79-61; E-mail:
[email protected]
of tumor removal was judged objectively according to the postoperative MRI examination performed within 24 h postoperatively. Patient records were retrospectively reviewed. Routine follow up in the clinic was obtained in the vast majority of patients. Others were evaluated with a telephone conversation to evaluate their functionality. Classical midline suboccipital and paramedian suboccipital approaches and the far-lateral transcondylar modification were used for tumor resection. For this pathology, no anterior approaches were utilized at our institution. Pre- and post-operative functionality of the patient was assessed both with the Karnofsky performance scale and according to the classification scheme proposed by Yasargil et al.26 (grade 0: asymptomatic, grade 1: single minor sign or symptom, grade 2: minor signs or symptoms, grade 3: marked signs, grade 4: bedridden patient, grade 5: dead).
RESULTS Between January 1990 and January 2003, twenty five patients were diagnosed with foramen magnum meningiomas. Of the surgically treated 22 patients, 4 (18%) were male and 18 (82%) were female. The median age was 47 (ranging from 18 to 74) and the mean age at diagnosis was 47.2 years (SD 16.9). Presenting signs and symptoms were headache and neck pain in 16 patients (73%), nausea and vomitting in 12 patients (55%), difficulty in swallowing in 7 patients (32%), monoparesis in 5 patients (23%), brachalgia and arm paresthesias in 4 patients(18%), dysarthria in 3 patients (14%), tongue hemiatrophy and fasciculations in 3 patients (14%), gait imbalance in one patient (5%) and quadriparesis in 2 patients. Mean duration of symptoms was 10 months (ranging from 1 to 72 months). Two patients were asymptomatic at hospitalization but were diagnosed on radiological grounds at follow up for other lesions. Two patients were diagnosed with neurofibromatosis (9%). 20/22 (91%) of the tumors were located anterolateral, 2/22 were posterior. Early in this series, a suboccipital approach was 863
864 Pamir et al.
performed in 3 patients (4%), 2 harboring posteriorly and 1 anterolaterally located tumors; and a far-lateral approach with partial removal of the occipital condyle was later utilized in 19 (96%) patients. However, the patient with anterolateral tumor, who was operated with suboccipital approach initially, revealed postoperative residual tumor and was reoperated with a far-lateral approach, resulting in radiological total tumor excision (Fig. 1). Partial resection of the lateral mass of C1 was done in all of the far-lateral approaches (Fig. 2). Even for large foramen magnum meningiomas, only drilling of the lateral 1/3 of the occipital condyle and/or 1/2 of the lateral mass of the atlas was required. No atlanto-occipital instability was observed in any of our patients. Surgical gross-total removal was achieved in 21 of these lesions (95.5%). The above mentioned patient, who was first op-
erated with a suboccipital craniotomy and then with the far-lateral approach for residual tumor, resulted in radiological total tumor excision. Another patient, who was operated with a far-lateral approach, had subtotal removal with adequate craniocervical decompression and eventually underwent gamma-knife radiosurgery for residual tumor. Operative finding of a very firm meningioma caused subtotal resection in this case. This patient remains functional at 120 months of follow up. No surgical mortality was observed in the cohort. CSF fistula occurred in 4 (18%) and all of these cases responded to lumbar drainage. One patient developed hydrocephalus and underwent a shunt procedure six months after hospital discharge. Transient lower cranial nerve palsies were seen in 2 patients which spontaneously resolved after two months. In one of these cases, the accesorius nerve was encased rather than displaced by the mass,
Fig. 1 Grading of the pre- and postoperative functional status at the latest follow up, according to the Yasargil classification. (Grade 0: asymptomatic, grade 1: single minor sign or symptom, grade 2: minor signs or symptoms, grade 3: marked signs, grade 4: bedridden patient, grade 5: dead.) Note the increase in the lower grades following surgery.
Fig. 2 Preoperative sagittal (A) and axial (D) contrast enhanced T1 weighted MRI examinations showing anterolateral type foramen magnum meningioma. Note the vertebral artery (arrow) encased in the tumor mass. Postoperative images (B, E) of the patient operated the paramedian approach with residual tumor. Postoperative with sagittal (C) and axial (F) contrast enhanced images taken after tumor removal with the far-lateral approach.
Journal of Clinical Neuroscience (2004) 11(8), 863–867
ª 2004 Elsevier Ltd. All rights reserved.
Foramen magnum meningiomas 865
making the excision of the involved nerve mandatory. The vertebral artery was encased in 9 cases and iatrogenic injury to the artery was seen in one patient during tumor dissection at the posterior inferior cerebellar artery take off. All but one case were typical meningiomas. One case was an atypical meningioma. Seventy two per cent of the tumors were meningothelial, 17% were transitional and 11% were psammomatous. Patients were followed for a median of 40 months (range: 2 months–10 years). At the latest follow up, 1 patient with neurofibromatosis (4.5%) was dead, 21 (95.5%) patients were alive and functionally independent. Mean Karnofsky score was 73 preoperatively and 94 at the latest follow up. Postoperative functional status according to the Yasargil classification is indicated in (Fig. 1). No recurrences were observed.
Fig. 3 Intraoperative photograph showing tumor exposure with the farlateral approach (A). Note that the extradural vertebral artery is skeletonized and retracted laterally and out of the field. c: cerebellum, d: dura, sc: spinal cord, p: posterior inferior cerebellar artery, t: tumor, va: intradural vertebral artery, X,XI,XII: cranial nerves 9,10 and 11. Pre- (B) and post-operative (C) axial contrast enhanced T1 weighted MRI images of the same patient showing gross-total surgical tumor removal. Postoperative 3D computerized tomography with internal (D) and external (E) views of the foramen magnum showing the extent of bone removal. Note that the occipital condyle is anatomically intact (arrow) (c1: atlas, c2: axis, cl: clivus, o: occiput, m: mastoid process, p: petrous ridge).
ª 2004 Elsevier Ltd. All rights reserved.
DISCUSSION According to George et al.,17 the first case report of a foramen magnum meningioma was described in 1872 by Halopeau at autopsy. This was followed in 1922 by Frazier and Spiller's14 first report of surgical removal. Since then foramen magnum meningiomas have always been an attractive topic among neurosurgeons. The interest was first focused on their puzzling symptomatology2;9;25;32 , but after the advent of advanced radiological technology38 the interest was directed toward the challenges dictated by their perplexing surgical anatomy. Cushing was the first to name the tumor11 and report a surgical series.12 Surgical reports of foramen magnum meningiomas have been sparse and mainly consist of case series of surgical pioneers.20;21;39;40 With their popularization and maturation in the last two decades, skull base approaches and their results have dominated the literature.4;8;10;13;16;18;24;31;33 These techniques have significantly expanded the neurosurgical armamentarium by increasing our surgical capabilities and decreasing morbidity. The female to male ratio of almost four to one is consistent with the literature.18 Comparison of the recent literature is given in Table 1. Several authors described classification schemes according to the zone of dural attachment of the tumor on the axial plane. These schemes help in defining the surgical approach. George et al.18 classified foramen magnum meningiomas into three groups according to their zone of insertion and used anterior, lateral and posterior approaches to foramen magnum lesions. Al-Mefty and colleagues5 classified foramen magnum meningiomas according to their site of origin and described craniospinal and spinocranial meningiomas. Meningiomas were classified as anterior if their zone of insertion was on both sides of the midline. Ventral foramen magnum meningiomas are the most challenging surgical group among meningiomas of this region. Arnautovic et al.5 reported that ventrally located foramen magnum meningiomas comprise 68–98% of the total and suggested that these lesions are different in their symptomatology, neurological findings, operative approach, postoperative results, complications and mortality rates. They also stressed that their challenging anatomy, in the vicinity of vital structures and cranial nerves, posed further surgical difficulties. Goel et al.19 suggested that even anterior foramen magnum meningiomas could be operated on with the median suboccipital approach. Their approach however involves the removal in part of the occipital condyle and therefore basically is a modification of the lateral approaches, not a conventional posterior approach. Our experience has shown that partial condylectomy, as a part of the far-lateral modification of the paramedian suboccipital approach, significantly increases the manoeuverability of the surgical instruments for anteriorly located lesions. Akba et al.1 have shown that the removal of the posteromedial portion of the occipital condyle beyond the hypoglossal canal provides a wider angle of exposure and decreases the working distance. This was later confirmed by the quantitative work of Spektor et al.36 However, several authors have stated that condylectomy becomes unnecessary in removal of large tumors, which provide the necessary visualization of anterior structures. The far-lateral approach provides exposure of the upper ventral spinal canal, anterior portion of the foramen magnum, lower and middle clivus and the jugular foramen (Fig. 3).36 Routine use of the far lateral approach for foramen magnum meningiomas started at Marmara University after 1992. The most devastating complications related to this approach are lower cranial nerve palsies and vertebral artery injury. Encasement of the vertebral artery was seen in 9 (40%) of our patients. In one patient, the vertebral artery was resected after preoperative planning. There was one (4.5%)
Journal of Clinical Neuroscience (2004) 11(8), 863–867
N/A None
None
14 0
43 months median/ maximum N/A N/A 40 months/10 years N/A
N/A 0 0 2/40 of all series 0 None N/A 2/18 N/A 4.3 years/7 years 10 months/19 months 21 months/10 years 4.8 years/10 years 4.8 years/0 years 14.8 months/50 months 64 months/84 months
N/A 30
N/A
72 95
82
0 0 75 30 of whole series 0 7.5 36 of whole series 55
29 0 13 6 0 0.75 0 0
0 0 0 N/A 10.2 years/14.2 years N/A/10 years N/A/34 years N/A 3.5 9 11 20 2.7 0 12 60
N/A 43 100 80 (40 at a second operation) 80 N/A 75 52 100 86 66 75
Scientific activities of T€ urker Kılıcß M D P H D have been financially supported by Turkish Academy of Sciences.
Journal of Clinical Neuroscience (2004) 11(8), 863–867
Series including other pathologies or involving other anatomical compartments are indicated.
2002 2003 Marin-Sanabria et al.24 Present series
7 22
2001
71 91
100 17
1993 1994 1994 1996 1996 1997 1999 2000
Kratimenos et al.23 Akalan et al.3 Babu et al.7 Samii et al.31 Bertalanfy et al.10 George et al.18 Salas et al.30 Arnautovic and Al-Mefty5 Goel et al.19
100 100 N/A 92 100 97.5 N/A 100 8 8 8 25 19 40 24 18
1978 1980 1988 1990 Yasuoka et al.40 Yasargil et al.39 Guidetti et al.20 Sen et al.34
80.7 N/A N/A 100
REFERENCES
37 23 17 5
Gross-total resection (%) Anterior and anterolateral lesions (%)
Surgery is effective in the treatment of foramen magnum meningiomas. The far-lateral modification has expanded the surgical armamentarium by increasing efficacy and minimizing morbidity. There is no single best approach for foramen magnum meningiomas. However, the optimal approach should be tailored according to the localization and the extent of the tumor bulk to minimize the extent of resultant morbidity. ACKNOWLEDGEMENT
Year
Number of cases
unexpected vertebral artery, injury in our series. In this case, a tear in the vertebral artery was caused during dissection and mobilization of the posterior inferior cerebellar artery. This is the only case in our series resulting in residual tumor after transcondylar approach. To decrease injury to the artery, exposure and subsequent mobilization of the V3 segment of the vertebral artery from C2 to the dural entry point was first described by George et al.15 At the craniovertebral junction, the vertebral artery is encased in a venous plexus. This plexus spans the area between the atlantooccipital membrane and the posterior fossa dura. Parkinson29 described its analogy with the lateral sellar compartment. This venous plexus was named the occipital cavernous sinus by Arnautovic et al.6 During dissection, bleeding from the plexus is easily controlled by packing and gentle compression, this also aids in the protection of the artery during surgical exposure. The most common pathological subtype was meningothelial meningioma. This is consistent with the prior literature.3–5;17–19;31;33;35;39 No association between the histological subtype and extent of resection or recurrence is reported for foramen magnum meningiomas. CONCLUSION
Author
Table 1
Recent major surgical series of foramen magnum meningiomas reported in the last 25 years (1978–2003)
Morbidity (%)
Surgical mortality (%)
Duration of follow up (mean/max)
Recurrence
866 Pamir et al.
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Journal of Clinical Neuroscience (2004) 11(8), 863–867