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Foramen magnum meningioma: The midline suboccipital subtonsillar approach
Clinical Neurology and Neurosurgery 145 (2016) 28–34
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Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Foramen magnum meningioma: The midline suboccipital subtonsillar approach S. Dobrowolski, F. Ebner, G. Lepski, M. Tatagiba ∗ Department of Neurosurgery, Eberhard Karl University, Tübingen, Germany
a r t i c l e
i n f o
Article history: Received 27 December 2015 Received in revised form 1 February 2016 Accepted 18 February 2016 Available online 2 April 2016 Keywords: Posterior fossa meningioma Foramen magnum Surgical approach Skull base
a b s t r a c t Objectives: Foramen magnum meningiomas (FMMs) represent a technical challenge even for experienced neurosurgeons, because they grow in close contact with osteoarticular, nervous, and vascular structures that cannot be sacrificed or retracted during surgery. Our goal is to present our experience with 24 cases of surgically resected foramen magnum meningiomas used the midline suboccipital subtonsillar approach and discussed the present risks associated with the treatment of this condition. Patients and methods: We retrospectively reviewed all patients who underwent surgery treatment for foramen magnum meningiomas operated on between August 2005 and July 2013. A total of 24 cases were included. Data regarding age, sex, symptoms and sign types, locations, surgical aspects, postoperative new deficits, and follow-up are presented. Results: There were 18 female and 6 male patients (mean age: 52 years). The symptom among most patients (14 patients) was cervico-occipital pain, dysphagia and gait unsteadiness in five, and paresthesia of the upper limbs in four. Total removal of the tumor was achieved in 20 patients, subtotal in two, and partial resection in four patients. Two patients had permanent deficits. Follow-up was 45.6 months (range, 6 months to 8 years), there was no recurrence among tumors totally removed but 1 patient of regrowth among the cases with subtotal removal. Conclusions: Our experience confirmed that the midline suboccipital subtonsillar approach was accurate in safely removing anterior, anterolateral, and posterior FMMs. There was no significant postoperative complication in the remainder of the patientes, and their conditions improved after surgery. © 2016 Elsevier B.V. All rights reserved.
1. Introduction Meningiomas are common neoplasms affecting the nervous system, and represent 20% of all primary intracranial tumors [1]. However, meningiomas arising in the foramen magnum (FMM) are rare, since they account for approaximately 1.5 to 3.2% of all intracranial meningiomas [2,3]. The choice for the best treatment depends on several factors, including tumor position, size, compression of neural structures and related symptoms, patient age, and morbidity conditions. Surgery remains the treatment of choice for patients in good general condition with symptomatc FMMs because it is the therapy that can cure the disease. However, in an era in which the high morbidity risk has become unacceptable for many patients and in which radiosurgery is under
∗ Corresponding author at: Departament of Neurosurgery, University of Tuebingen Hoppe-Seyler-Str., 3 72076 Tuebingen, Germany. E-mail addresses: [email protected], [email protected] (M. Tatagiba). http://dx.doi.org/10.1016/j.clineuro.2016.02.027 0303-8467/© 2016 Elsevier B.V. All rights reserved.
evaluation as a potentially safe and effective alternative for poor candidates for resection. Conservative management might be preferred in elderly patientes with mild symptoms [4]. Should surgery be considered, there is currently no consensus regarding the ideal approach [5–10]. In addition to the standard midline suboccipital craniotomy and upper cervical laminectomy [11,12], several surgical approaches have been proposed for resection of such tumors. These approaches include the anterior transoral [6], lateral trans-cervical [7], and posterolateral suboccipital [8]. Taken into consideration that some of these surgical series date back more than 20 years, we consider relevant the description of the current risks associated with surgery, in light of the recent refinements in the surgical technique, in electrophysiological monitoring, and neuro-anaesthesiology, to allow the proposition of an actualized treatment algorithm. Here we report 24 cases of meningiomas arising in the foramen magnum, as defined by Bruneau [2] (i.e., tumors arising anteriorly from the inferior third of the clivus to the superior edge of the C2 body, laterally form the jugular tubercle to the C2 laminae, and posteriorly from the anterior border of the occipital squama
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to the spinal process of C2). Moreover, we reviewed the pertinent literature regarding the current management of FMM and the treatment-associated risks.
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2. Patients and methods
hallucis muscles were recorded. Additionally, MEPs from the mimic muscles (facial nerve, m. orbicularis oris e oculi), auditory evoked potentials, as well as MEPs from the pharynx (vagal and glossopharyngeal nerves), and tongue (hypoglossal nerve) were also recorded (C4-Cz for the left body side and C3-Cz for the right side, 150–250 V).
2.1. Patient population
2.5. Surgical technique
During an 8-year period from August 2005 to July 2013, all patients who underwent microsurgery for FMM in the neurosurgical department at the University of Tübingen, in Germany were included in this study, a total of 24 patients. All patients harboured meningiomas arising primary from the anterior, anterolateral or posterior dura at the foramen magnum level, being confined within the following boundaries, as described previously [2]: anteriorly, lower third of the clivus to upper edge of axis; laterally, jugular tubercle to upper aspect of the C2 laminae; and posteriorly, anterior edge of the squamous occipital bone to the C2 spinous process. The medical chats were reviewed with respect to the clinical, radiological, and surgical aspects of these tumors, as well as the outcome after mid-term follow.
During surgery, anaesthesia was maintained intravenously with 1% Propofol and Remifentanyl. To avoid interference with neurophysiological monitoring, inhaled anaesthetic agents and muscle-relaxing drugs was not used. Effort was made to keep body temperature constant with a thermic mantle; oscillations of the mean arterial pressure were promptly corrected with Norepinephrine. As previously described [18–20], we favored the semi-sitting position under continuous trans-oesophageal echocardiographicmonitoring (2.2 MHz) for recognition of any venous air embolism. To this end, Anaesthesiological monitoring also included a central venous catheter placed in the right atrium, continuous invasive blood pressure measurement with a radial artery catheter, electrocardiogram, pulse oximetry, and capnography with end-tidal CO2 . In this position, the veins are less turgid, and the cerebellar parenchyma less oedematous. Moreover, CSF-drainage of the basal cisterns permits a gentile retraction of the cerebellum without major trauma, and the assistant can perform continuous irrigation of the blood from the operation field while the surgeon works on the tumour (four-hand technique). A midline vertical skin incision is made from the inion to the second vertebral lamina and a burr hole is made over the external occipital protuberance. The craniotomy is directed toward the foramen magnum, which is then opened. The posterior arch of the C1 is removed. The dura is opened under the surgical microscope in a Y-like fashion. The arachnoid membrane is incised, which releases additional CSF and allow for less retraction of the cerebellum. By providing an ample and direct corridor, the subtonsillar approach allows for tumor removal under excellent control of the surrounding structures, including the ventral most part of the operation field. The tumor is initially debulked up to the brainstem, and sequentially dissected from the lower cranial nerves and vertebral artery. After tumor resection is completed, meticulous haemostasis is carried out. The dura mater is closed in a watertight fashion and the bone defect is reconstructed with methyl-metacrylate. The muscle layers are closed in the standard fashion.
2.2. Neuroimaging studies Neuroradiological workup included contrast-enhanced magnetic resonance imaging (MRI) in all 24 patients. MRI scans accurately delineated the exact tumor size, location, site of dural attachment, and relationship to vascular and neural structures; moreover, MRI also provides cues about consistency and vascularity of the tumor. Thin-sliced computed tomography (CT) scans of the FM region were performed in 5, and complete cerebral angiography were obtained in five patients. (Fig. 1). 2.3. Classification of FMM Based on the sagital MRI films, the tumors originating from the clivus and extending caudally to the foramen magnum with a dural tail in the clivus were classified as clivospinal, whereas the tumors arising from the spinal canal and extending upward to the foramen magnum were classified as spinoclival. Based on the axial MRI scans, tumors were classified as: (i) anterior, if attached to the anterior rim of the FM and displaced the neuraxis in a purely posterior direction, (ii) anterolateral, if the attachment was on the ventrolateral rim of the FM, thus displacing the neuraxis posterolaterally, and (iii) posterior, if the attachment was posterior to the dentate ligament. 2.4. Electrophysiological assessment A detailed description of our electrophysiological routine is described elsewhere [13–17]. Electrophysiological recordings were carried on in all cases using a Nicolet Endeavour CR (Cardinal Health, Dublin, Ireland). Before craniotomy, bilateral tibial and median nerve somatosensory evoked potentials (SEPs) were elicited by conventional stimulation at the ankle and wrist, respectively (20–40 mA, duration 0.2 milliseconds, 3.1–5.2 Hz) and recorded via scalp corkscrew electrodes placed over the primary sensory cortex. Transcranial motor evoked potentials (MEPs) were elicited with a constant-voltage stimulator (D185, Digitimer Ltd.) using corkscrew electrodes placed over the primary motor cortex (for left body side C4 against C3; for right body side C3 against C4). Stimulation was performed using 5 pulses of 400 to 600 V, 50millisecond pulse duration, and an inter-stimulus interval of 2–4 milliseconds. For the upper limbs, contralateral muscle responses were recorded with needle electrodes inserted in the hypotenar and tenar muscles. For the lower limbs, responses of the abductor
2.6. Patient follow-up All patients were followed up with clinical examination and MRI studies 6 months and 1 year after surgery. Thereafter, patients were reevaluated at 1 year intervals. The extent of tumors resection was based on postoperative MRI finding and defined as total (absence of residual tumor or dural enhancement), subtotal (absence of tumor but presence of dural enhancement), and partial (presence of residual tumor). 3. Results 3.1. Clinical data Eighteen women and six men were included in the present series. Mean age was 52 years (range 10–82 years). The more common symptoms were cervico-occipital pain in 14 patients, dysphagia and gait unsteadiness in five, and paresthesia of the upper limbs in four. At the neurological examination by admission, limb hypesthesia was encountered in four patients, monoparesis in three, hemiparesis in two, tetraparesis in another two patients and
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Fig. 1. Neuroradiology findings. (A) Sagittal fast fluid attenuated inversion recovery (FLAIR) image demonstrates intradural mass at right foramen magnum resulting in slight displacement of the medulla and transdural hypoglossal canal involvement. (B) Sagittal contrast-enhanced T1-weighted spin echo (SE) image demonstrates intradural mass at foramen magnum. Neuroradiology finding. (C) Axial CT. Preoperative calcified mass at right foramen magnum resulting in slight displacement of the medulla. (D) Axial postoperative CT showing no residual tumor and bone resection.
triparesis in only one. Cranial nerve deficits were encountered in four patients, including concomitant paresis of the glossopharyngeal and vagus nerves in four patients, additional accessory nerve paresis in two of them, and one patient out of these two presented also an hypoglossal nerve deficit. (Table 1). The mean preoperative Karnofsky Performance Scale score (KPS) was 85 (range 70–100) [21].
3.2. Surgical aspects The midline suboccipital subtonsillar approach was used in all cases presented here. However, the extent of bone removal and the management of the vertebral artery were different in each case. The extent of tumor resection according to Simpson’s scale was grade I in four patients, grade II in 15 patients, grade III in one patient, and grade IV in four patients [22]. The occipital condyle was partially removed in two cases (only the posterior third).
Tumors that had encased the vertebral artery could be removed safely along an arachnoid dissection plane. Displacement of the artery was necessary in sixteen cases during resection. In the remaining 8 cases, the vertebral artery was left intact (Table 2).
3.3. Radiological outcome Total removal of the tumor was achieved in 20 patients, whereas the resection was subtotal in the remaining four. The first patient with subtotal removal was a 47-year-old male with rhabdoid meningioma, which extended extradurally invading the vertebral artery and expanding intradurally to the jugular foramen. The second patient was a 52-year-old female with a meningioma with en plaque extension and extradural growth and strongly attached in the neural and vascular structures. The third patient was a 51-yearold male with Neurofibromatosis Type II, who had been operated on a accessorius neurinoma in the cerebellopontine angle with craniocervical extension 5 years before. The fourth patient was
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Table 1 Preoperative symptoms and neurological sign in 24 patients with FMM.
a 51-year-old female; during her surgery, constant spontaneous evoked electromyographic responses were elicited in the lower cranial nerves, so that we decided to leave some residual tumor to avoid definitive lower cranial nerve deficits. The average length of follow-up was 45.6 months (range, 6 months to 8 years), there was no recurrence among tumors totally removed but 1 patient of regrowth among the cases with subtotal removal. 3.4. Surgical morbidity Postoperative complications occurred in three patients. A 45 year-old female with a 2.8 cm clivospinal anteriolateral tumor encasing the vertebral artery presented a postoperative hemorrhage probably related to vessel injury; a surgical evacuation was necessary. Later, the same patient developed, CSF leak and hydrocephalus, which was managed with ventriculoperitoneal shunt implantation. The second patient was a 52 year-old female with a 3.8 cm spinoclival anterolateral tumor, which was ensheathing the accessory nerve, sectioned during tumor dissection. In the same procedure, an end-to-end reconstruction by means of sural grafts interposition was performed. In the postoperative period, the patient developed pneumonia and spontaneous thrombosis of the transverse sinus. The other serious morbidity occurred on a 13 year-old male with a 1.7 cm clivospinal anterolateral recurrent tumor and diagnosed with neurofibromatosis type II. The patient had been previously submitted to surgical resection of a large accessorius neurinoma in the cerebellopontine angle with craniocervical extension. After the surgery the patient developed a slight transient dysphagia. There were no significant postoperative complications in the other patients. All patients improved in their motor power. Paresthesia and sensory deficits resolved completely in five patients (20%). In three patients, both the dysesthesia and sensory deficits persisted, thought to a significantly lesser extent. The most dramatic recovery was from the motor weakness. Three patients who had already dysphagia prior to surgery evolved with transient impairment. Due to the previous functional
deficit, the limitation has been fully compensated in all cases in a short term. For such cases, we routinely performed fiberendoscopic inspection of the vocal cord function immediately after extubation to avoid aspirative pneumonia.
4. Discussion Meningiomas arising at the foramen magnum have a slowly progressive clinical course, leading to dysesthesia, asymmetric motor weakness, gait ataxia, and, less commonly, lower cranial nerve affection. MRI consists the gold standard method for proper diagnosis and treatment planning. FMMs are known for their close relationship with important vascular, nervous and bone-articular structures. As a direct consequence, a great number of different surgical approaches have been described in the literature [4,6,7,9,23–26]. Anterior approaches, such as transoral or transcervical, are widely accepted for resection of extradural or ventrally-located tumors in the foramen magnum region [4,6,9]. The main advantage of the transoral approach is its direct route to the anterior foramen magnum. Possible complications include craniocervical instability, velopalatine insufficiency, a higher risk of postoperative cerebrospinal fluid leakage, and meningitis. In our experience, the complications far outweigh the benefits [18]. Moreover, FMM located strictly ventral to the brainstem are relatively rare, since they have often lateral extensions [23]. The transcervical retropharyngeal approach is usually favored in extradural lesions, but it is not widely used because complete resections in rostrally and laterally-extending tumors are troublesome and technically difficult [27]. Lateral approaches like the pre-sigmoid and transpetrosal include an extensive bone removal and high risk of injury to the seventh and eighth cranial nerves, especially if trans-cochlear drilling is necessary. In contrast, the posterior suboccipital midline approach is an easy and straightforward option. Vertebral arteries and cranial nerves are well manageable and, compared with the trans-oral or trans-cervical variants, the operation field is much
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Table 2 Clinical and radiological characteristics of 24 patients with FMMs. Symptom
Sign
Location size cm
Condyle removal
Vertebral artery
Remotion simpson
Postperative new deficts
Follow up
1
47y, M
Hemiparesis right, gait ataxia
Spinoclival anteriolateral right 3,6
No
Exposed and displaced
IV
45y, F
No
Exposed and displaced
II
82 months; No recurrence
3
72y, F
No
Exposed and displaced
III
No
78 months; No regrowth
4
52y, F 44y, F
Clivospinal anteriolateral right 2,8 Clivospinal Paresis upper limb left anterolateral Left 2,0 Tetraparesis, gait ataxia Clivospinal anteriolateral left 2,0 Slight IX, X cranial nerves Clivospinal deficits posterolateral right 2,2 Slight triparesis, gait ataxia Clivospinal anterior 2,5
Slight impairment of previous deficits of the hemiparesis No
94 months; No recurrence
2
Cervical pain, motor weakness, gait unsteadiness Cervical pain
No
Exposed and displaced
I
No
53 months; No recurrence
Yes, 1/3 post. Condyle
Exposed and untouched
I
Slight dysphagia
46 months; No recurrence
Yes, 1/3 post. Condyle
Exposed and displaced
II
Clivospinal posterior 2,0
No
Exposed and displaced
II
Clivospinal posterolateral right 3,3 Spinoclival anterolateral right 3,8 Clivospinal anterolateral left 2 cm Spinoclival anterolateral right 4,2
No
Exposed and displaced
I
46 months; No recurrence Slight impairment of previous deficit (transitory) Xth cranial nerve unilateral 32 months; No recurrence (transitory) No 36 months; No recurrence
No
Exposed and displaced
IV
No
30 months; No regrowth
No
Exposed and untouched
I
No
28 months; No recorrence
No
Exposed and displaced
II
No
28 months; No recorrence
Clivospinal anterolateral left 3,0
No
Exposed and displaced
II
No
20 months; No recorrence
Clivospinal lateral right 2,0 No Clivospinal lateral left 3,0 No
Exposed and displaced Exposed and displaced
II II
No Slight transient hypoglossal paresis
8 months; No regrowth 6 months; No recorrence
Spinoclival anterolateral left 1,5 Spinoclival anterolateral left 2,5 Spinoclival anterolateral left 1,5 Clivospinal anterolateral left 2,7 Clivospinal anterior 1,5 Spinoclival anterolateral left 2,8
No
Exposed and untouched
II
No
82 months; No recorrence
No
Exposed and displaced
II
No
78 months; No recorrence
No
Exposed and displaced
II
No
76 months; No recorrence
No
Exposed and untouched
II
No
73 months; No recorrence
No No
Exposed and untouched Exposed and untouched
II II
No Slight transient paresis upper left limb
72 months; No recorrence 54 months; No recorrence
No Clivospinal anterolateral right 1,7 Clivospinal lateral right 3,0 No
Exposed and displaced
IV
Slight transient dysphagia
48 months; regrowth
Exposed and untouched
II
26 months; No recorrence
Clivospinal anterior 2,0
No
Exposed and displaced
IV
Slight transient Lower motor neurone dysarthria and dysphagia No
23 months; No regrowth
Clivospinal posterior 2,6
No
Exposed and untouched
II
No
21 months; No recorrence
5
Occipital pain, vertigo, diplopia Occipital pain Occipital pain, slight dysphagia, visual disturbance Cervical pain; parasthesia upper limb, motor weakness, Cervical pain, dysphagia, gait unsteadiness Motor weakness
Slight paresis upper limb
6
61y, F
7
69F
8
74F
9
52F
10
82F
11
42F
12
64F
13 14
27y, M 46y, F
15
55y, F
Cervical pain, shouder pain, IX, X, XI, XII cranial nerves dysphagia, hoarseness deficits Cervical pain, dysphagia IX, X, XI cranial nerves deficits Hypesthesia, paresis upper Slight paresthesia upper limb right, motor limb weakness Tetraparesis, gait ataxia Cervical pain, slight dysphagia, gait unsteadiness No deficits No symptom Cervical pain, disesthesia Gait ataxia face, gait unsteadiness, urge incontinence No symptom No deficits
16
54y, M
Vertigo
17
45, M
No symptom
Slightly horizontal nystagnus No deficits
18
45, F
Cervical pain
Hypesthesia
19 20
10y, F 51y, F
21
13y, M
No symptom No deficits Hypesthesia Cervical pain, slight paresthesia upper limb left, motor weakness No symptom No deficits
22
81y, F
Occipital pain
23
51y, M
24
55y, F
Paresthesia bilateral upper Gait ataxia limbs, with predominant right, gait unseadiness No symptom No deficits
IX, X, XI cranial nerve deficit Hemiparesis right
Hypesthesia
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Patient Age/sex
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wider and not so deep. For tumors located exclusively ventral to the brainstem, the approach can be extended laterally [18]. Several lateral modifications have been described, like the far-lateral with or without transcondylar extension [3,25]. In our experience, a midline suboccipital craniotomy with no drilling of the posterior third of the occipital condyle proved to be sufficient to expose the ventral part of the foramen magnum region, with the main advantage of offering an operation field not so deep as compared with that obtained by trans-cervical, trans-oral, and even lateral approaches. The far-lateral transcondylar approach involves exposure of the transverse process of C1. However, it is more time-consuming and implies higher risks of CSF-leakage and (always) cranio-cervical instability. The far-lateral supracondylar approach, instead, is tailored to the area above the occipital condyle, and similarly permits exposition of the foramen magnum and clival areas. In special cases, neck dissection may be necessary [24]. The far-lateral approaches provide lateral exposure of the brainstem, thus permitting a safe dissection without significant retraction. The entire longitudinal and lateral extensions of the tumor, as well as eventual extra-dural components, can be achieved using this approach [25]. The main drawback is the aggressive bone removal necessary. Some variations desired to overcome this drawback, like the retrocondylar approach, involve only partial occipital condyle drilling and do not cause any craniocervical instability [28]. Posterior and posterolateral FMMs can be safely resected via a standard midline suboccipital approach. Controversy still exits, however, regarding the optimal management of ventral or ventrolateral lesions. In those cases, surgery could result in undue brainstem retraction, higher rates of subtotal resection (STR), and postoperative morbidity, due to inadequate exposure [5,29,30]. It has been suggested that patients operated on via conventional suboccipital approaches have worse clinical outcomes than patients operated on via the transcondylar route [5,9,26]. Those findings were contested by Goel et al., who reported gross-total resection (GTR) of 14 anterior or anterolateral FMMs through a conventional posterior suboccipital approach, similar to the results obtained by other authors [18,31,32]. Our experience confirmed that the midline suboccipital subtonsillar approach was accurate in safely removing anterior, anterolateral, and posterior FMMs. There was no significant postoperative complication in the remainder of the patientes, and their conditions improved after surgery.
5. Conclusion Conclusively, the subtonsillar approach provides excellent access, allowing a direct view of the foramen of Luschka laterally and up to the middle cerebellar peduncle [33]. In addition, the STA takes into consideration the anatomical displacement commonly caused by the lesion, providing a direct route to the same. Radical resection of the lesion – even of its extra-cranial parts – is feasible and safe with a standard craniotomy, which does not require additional time for bone drilling. Moreover, extradural problems can be avoided, such as dealing with the jugular bulb or with the jugular foramen. The STA is limited, however, in tumors extending too far inferiorly. In these cases, additional neck dissection is usually advisable [20].
Declaration of interest The authors state that they have no conflicts of interest to disclose. The authors alone are responsible for the content and writing of the paper, and have all agreed with its content.
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Acknowledgments The authors would like to thank the research funding agencies CAPES Brazil for the financial support with a research scholarship.
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[25] C.N. Sen, L.N. Sekhar, An extreme lateral approach to intradural lesions of the cervical spine and foramen magnum, Neurosurgery 27 (August (2)) (1990) 197–204, PMID: 2385336. [26] C.N. Sen, L.N. Sekhar, Surgical management of anteriorly placed lesions at the craniocervical junction—an alternative approach, Acta Neurochir. (Wien) 108 (1991) 70–77. [27] A.H. Menezes, V.C. Traynelis, B.J. Gantz, Surgical approaches to the craniovertebral junction, Clin. Neurosurg. 41 (1994) 187–203, PMID: 7842603. [28] R.J. Komotar, B.E. Zacharia, R.A. McGovern, M.B. Sisti, J.N. Bruce, A.L. D’Ambrosio, Approaches to anterior and anterolateral foramen magnum lesions: a critical review, J. Craniovertebr. Junct. Spine 1 (July (2)) (2010) 86–99, http://dx.doi.org/10.4103/0974-8237.77672. [29] B. George, G. Lot, H. Boissonnet, Meningioma of the foramen magnum: a series of 40 cases, Surg. Neurol. 47 (1997) 371–379.
[30] J.M. Gilsbach, Extreme lateral approach to intradural lesions of the cervical spine and foramen magnum, Neurosurgery 28 (1991) 779 (Letter). [31] A. Goel, K. Desai, D. Muzumdar, Surgery on anterior foramen magnum meningiomas using a conventional posterior suboccipital approach: a report on an experience with 17 cases, Neurosurgery 49 (July (1)) (2001) 102–106, discussion 106-107. Review. PMID: 11440430. [32] S.K. Gupta, V.K. Khosla, R. Chhabra, K.K. Mukherjee, Poste- rior midline approach for large anterior/anterolateral foramen magnum tumours, Br. J. Neurosurg. 18 (2004) 164–167. [33] W.C. Jean, K.M. Abdel Aziz, J.T. Keller, H.R. van Loveren, Subtonsillar approach to the foramen of Luschka: an anatomic and clinical study, Neurosurgery 52 (April (4)) (2003) 860–866, discussion 866.
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Clinical Neurology and Neurosurgery journal homepage: www.elsevier.com/locate/clineuro
Foramen magnum meningioma: The midline suboccipital subtonsillar approach S. Dobrowolski, F. Ebner, G. Lepski, M. Tatagiba ∗ Department of Neurosurgery, Eberhard Karl University, Tübingen, Germany
a r t i c l e
i n f o
Article history: Received 27 December 2015 Received in revised form 1 February 2016 Accepted 18 February 2016 Available online 2 April 2016 Keywords: Posterior fossa meningioma Foramen magnum Surgical approach Skull base
a b s t r a c t Objectives: Foramen magnum meningiomas (FMMs) represent a technical challenge even for experienced neurosurgeons, because they grow in close contact with osteoarticular, nervous, and vascular structures that cannot be sacrificed or retracted during surgery. Our goal is to present our experience with 24 cases of surgically resected foramen magnum meningiomas used the midline suboccipital subtonsillar approach and discussed the present risks associated with the treatment of this condition. Patients and methods: We retrospectively reviewed all patients who underwent surgery treatment for foramen magnum meningiomas operated on between August 2005 and July 2013. A total of 24 cases were included. Data regarding age, sex, symptoms and sign types, locations, surgical aspects, postoperative new deficits, and follow-up are presented. Results: There were 18 female and 6 male patients (mean age: 52 years). The symptom among most patients (14 patients) was cervico-occipital pain, dysphagia and gait unsteadiness in five, and paresthesia of the upper limbs in four. Total removal of the tumor was achieved in 20 patients, subtotal in two, and partial resection in four patients. Two patients had permanent deficits. Follow-up was 45.6 months (range, 6 months to 8 years), there was no recurrence among tumors totally removed but 1 patient of regrowth among the cases with subtotal removal. Conclusions: Our experience confirmed that the midline suboccipital subtonsillar approach was accurate in safely removing anterior, anterolateral, and posterior FMMs. There was no significant postoperative complication in the remainder of the patientes, and their conditions improved after surgery. © 2016 Elsevier B.V. All rights reserved.
1. Introduction Meningiomas are common neoplasms affecting the nervous system, and represent 20% of all primary intracranial tumors [1]. However, meningiomas arising in the foramen magnum (FMM) are rare, since they account for approaximately 1.5 to 3.2% of all intracranial meningiomas [2,3]. The choice for the best treatment depends on several factors, including tumor position, size, compression of neural structures and related symptoms, patient age, and morbidity conditions. Surgery remains the treatment of choice for patients in good general condition with symptomatc FMMs because it is the therapy that can cure the disease. However, in an era in which the high morbidity risk has become unacceptable for many patients and in which radiosurgery is under
∗ Corresponding author at: Departament of Neurosurgery, University of Tuebingen Hoppe-Seyler-Str., 3 72076 Tuebingen, Germany. E-mail addresses: [email protected], [email protected] (M. Tatagiba). http://dx.doi.org/10.1016/j.clineuro.2016.02.027 0303-8467/© 2016 Elsevier B.V. All rights reserved.
evaluation as a potentially safe and effective alternative for poor candidates for resection. Conservative management might be preferred in elderly patientes with mild symptoms [4]. Should surgery be considered, there is currently no consensus regarding the ideal approach [5–10]. In addition to the standard midline suboccipital craniotomy and upper cervical laminectomy [11,12], several surgical approaches have been proposed for resection of such tumors. These approaches include the anterior transoral [6], lateral trans-cervical [7], and posterolateral suboccipital [8]. Taken into consideration that some of these surgical series date back more than 20 years, we consider relevant the description of the current risks associated with surgery, in light of the recent refinements in the surgical technique, in electrophysiological monitoring, and neuro-anaesthesiology, to allow the proposition of an actualized treatment algorithm. Here we report 24 cases of meningiomas arising in the foramen magnum, as defined by Bruneau [2] (i.e., tumors arising anteriorly from the inferior third of the clivus to the superior edge of the C2 body, laterally form the jugular tubercle to the C2 laminae, and posteriorly from the anterior border of the occipital squama
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to the spinal process of C2). Moreover, we reviewed the pertinent literature regarding the current management of FMM and the treatment-associated risks.
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2. Patients and methods
hallucis muscles were recorded. Additionally, MEPs from the mimic muscles (facial nerve, m. orbicularis oris e oculi), auditory evoked potentials, as well as MEPs from the pharynx (vagal and glossopharyngeal nerves), and tongue (hypoglossal nerve) were also recorded (C4-Cz for the left body side and C3-Cz for the right side, 150–250 V).
2.1. Patient population
2.5. Surgical technique
During an 8-year period from August 2005 to July 2013, all patients who underwent microsurgery for FMM in the neurosurgical department at the University of Tübingen, in Germany were included in this study, a total of 24 patients. All patients harboured meningiomas arising primary from the anterior, anterolateral or posterior dura at the foramen magnum level, being confined within the following boundaries, as described previously [2]: anteriorly, lower third of the clivus to upper edge of axis; laterally, jugular tubercle to upper aspect of the C2 laminae; and posteriorly, anterior edge of the squamous occipital bone to the C2 spinous process. The medical chats were reviewed with respect to the clinical, radiological, and surgical aspects of these tumors, as well as the outcome after mid-term follow.
During surgery, anaesthesia was maintained intravenously with 1% Propofol and Remifentanyl. To avoid interference with neurophysiological monitoring, inhaled anaesthetic agents and muscle-relaxing drugs was not used. Effort was made to keep body temperature constant with a thermic mantle; oscillations of the mean arterial pressure were promptly corrected with Norepinephrine. As previously described [18–20], we favored the semi-sitting position under continuous trans-oesophageal echocardiographicmonitoring (2.2 MHz) for recognition of any venous air embolism. To this end, Anaesthesiological monitoring also included a central venous catheter placed in the right atrium, continuous invasive blood pressure measurement with a radial artery catheter, electrocardiogram, pulse oximetry, and capnography with end-tidal CO2 . In this position, the veins are less turgid, and the cerebellar parenchyma less oedematous. Moreover, CSF-drainage of the basal cisterns permits a gentile retraction of the cerebellum without major trauma, and the assistant can perform continuous irrigation of the blood from the operation field while the surgeon works on the tumour (four-hand technique). A midline vertical skin incision is made from the inion to the second vertebral lamina and a burr hole is made over the external occipital protuberance. The craniotomy is directed toward the foramen magnum, which is then opened. The posterior arch of the C1 is removed. The dura is opened under the surgical microscope in a Y-like fashion. The arachnoid membrane is incised, which releases additional CSF and allow for less retraction of the cerebellum. By providing an ample and direct corridor, the subtonsillar approach allows for tumor removal under excellent control of the surrounding structures, including the ventral most part of the operation field. The tumor is initially debulked up to the brainstem, and sequentially dissected from the lower cranial nerves and vertebral artery. After tumor resection is completed, meticulous haemostasis is carried out. The dura mater is closed in a watertight fashion and the bone defect is reconstructed with methyl-metacrylate. The muscle layers are closed in the standard fashion.
2.2. Neuroimaging studies Neuroradiological workup included contrast-enhanced magnetic resonance imaging (MRI) in all 24 patients. MRI scans accurately delineated the exact tumor size, location, site of dural attachment, and relationship to vascular and neural structures; moreover, MRI also provides cues about consistency and vascularity of the tumor. Thin-sliced computed tomography (CT) scans of the FM region were performed in 5, and complete cerebral angiography were obtained in five patients. (Fig. 1). 2.3. Classification of FMM Based on the sagital MRI films, the tumors originating from the clivus and extending caudally to the foramen magnum with a dural tail in the clivus were classified as clivospinal, whereas the tumors arising from the spinal canal and extending upward to the foramen magnum were classified as spinoclival. Based on the axial MRI scans, tumors were classified as: (i) anterior, if attached to the anterior rim of the FM and displaced the neuraxis in a purely posterior direction, (ii) anterolateral, if the attachment was on the ventrolateral rim of the FM, thus displacing the neuraxis posterolaterally, and (iii) posterior, if the attachment was posterior to the dentate ligament. 2.4. Electrophysiological assessment A detailed description of our electrophysiological routine is described elsewhere [13–17]. Electrophysiological recordings were carried on in all cases using a Nicolet Endeavour CR (Cardinal Health, Dublin, Ireland). Before craniotomy, bilateral tibial and median nerve somatosensory evoked potentials (SEPs) were elicited by conventional stimulation at the ankle and wrist, respectively (20–40 mA, duration 0.2 milliseconds, 3.1–5.2 Hz) and recorded via scalp corkscrew electrodes placed over the primary sensory cortex. Transcranial motor evoked potentials (MEPs) were elicited with a constant-voltage stimulator (D185, Digitimer Ltd.) using corkscrew electrodes placed over the primary motor cortex (for left body side C4 against C3; for right body side C3 against C4). Stimulation was performed using 5 pulses of 400 to 600 V, 50millisecond pulse duration, and an inter-stimulus interval of 2–4 milliseconds. For the upper limbs, contralateral muscle responses were recorded with needle electrodes inserted in the hypotenar and tenar muscles. For the lower limbs, responses of the abductor
2.6. Patient follow-up All patients were followed up with clinical examination and MRI studies 6 months and 1 year after surgery. Thereafter, patients were reevaluated at 1 year intervals. The extent of tumors resection was based on postoperative MRI finding and defined as total (absence of residual tumor or dural enhancement), subtotal (absence of tumor but presence of dural enhancement), and partial (presence of residual tumor). 3. Results 3.1. Clinical data Eighteen women and six men were included in the present series. Mean age was 52 years (range 10–82 years). The more common symptoms were cervico-occipital pain in 14 patients, dysphagia and gait unsteadiness in five, and paresthesia of the upper limbs in four. At the neurological examination by admission, limb hypesthesia was encountered in four patients, monoparesis in three, hemiparesis in two, tetraparesis in another two patients and
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Fig. 1. Neuroradiology findings. (A) Sagittal fast fluid attenuated inversion recovery (FLAIR) image demonstrates intradural mass at right foramen magnum resulting in slight displacement of the medulla and transdural hypoglossal canal involvement. (B) Sagittal contrast-enhanced T1-weighted spin echo (SE) image demonstrates intradural mass at foramen magnum. Neuroradiology finding. (C) Axial CT. Preoperative calcified mass at right foramen magnum resulting in slight displacement of the medulla. (D) Axial postoperative CT showing no residual tumor and bone resection.
triparesis in only one. Cranial nerve deficits were encountered in four patients, including concomitant paresis of the glossopharyngeal and vagus nerves in four patients, additional accessory nerve paresis in two of them, and one patient out of these two presented also an hypoglossal nerve deficit. (Table 1). The mean preoperative Karnofsky Performance Scale score (KPS) was 85 (range 70–100) [21].
3.2. Surgical aspects The midline suboccipital subtonsillar approach was used in all cases presented here. However, the extent of bone removal and the management of the vertebral artery were different in each case. The extent of tumor resection according to Simpson’s scale was grade I in four patients, grade II in 15 patients, grade III in one patient, and grade IV in four patients [22]. The occipital condyle was partially removed in two cases (only the posterior third).
Tumors that had encased the vertebral artery could be removed safely along an arachnoid dissection plane. Displacement of the artery was necessary in sixteen cases during resection. In the remaining 8 cases, the vertebral artery was left intact (Table 2).
3.3. Radiological outcome Total removal of the tumor was achieved in 20 patients, whereas the resection was subtotal in the remaining four. The first patient with subtotal removal was a 47-year-old male with rhabdoid meningioma, which extended extradurally invading the vertebral artery and expanding intradurally to the jugular foramen. The second patient was a 52-year-old female with a meningioma with en plaque extension and extradural growth and strongly attached in the neural and vascular structures. The third patient was a 51-yearold male with Neurofibromatosis Type II, who had been operated on a accessorius neurinoma in the cerebellopontine angle with craniocervical extension 5 years before. The fourth patient was
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Table 1 Preoperative symptoms and neurological sign in 24 patients with FMM.
a 51-year-old female; during her surgery, constant spontaneous evoked electromyographic responses were elicited in the lower cranial nerves, so that we decided to leave some residual tumor to avoid definitive lower cranial nerve deficits. The average length of follow-up was 45.6 months (range, 6 months to 8 years), there was no recurrence among tumors totally removed but 1 patient of regrowth among the cases with subtotal removal. 3.4. Surgical morbidity Postoperative complications occurred in three patients. A 45 year-old female with a 2.8 cm clivospinal anteriolateral tumor encasing the vertebral artery presented a postoperative hemorrhage probably related to vessel injury; a surgical evacuation was necessary. Later, the same patient developed, CSF leak and hydrocephalus, which was managed with ventriculoperitoneal shunt implantation. The second patient was a 52 year-old female with a 3.8 cm spinoclival anterolateral tumor, which was ensheathing the accessory nerve, sectioned during tumor dissection. In the same procedure, an end-to-end reconstruction by means of sural grafts interposition was performed. In the postoperative period, the patient developed pneumonia and spontaneous thrombosis of the transverse sinus. The other serious morbidity occurred on a 13 year-old male with a 1.7 cm clivospinal anterolateral recurrent tumor and diagnosed with neurofibromatosis type II. The patient had been previously submitted to surgical resection of a large accessorius neurinoma in the cerebellopontine angle with craniocervical extension. After the surgery the patient developed a slight transient dysphagia. There were no significant postoperative complications in the other patients. All patients improved in their motor power. Paresthesia and sensory deficits resolved completely in five patients (20%). In three patients, both the dysesthesia and sensory deficits persisted, thought to a significantly lesser extent. The most dramatic recovery was from the motor weakness. Three patients who had already dysphagia prior to surgery evolved with transient impairment. Due to the previous functional
deficit, the limitation has been fully compensated in all cases in a short term. For such cases, we routinely performed fiberendoscopic inspection of the vocal cord function immediately after extubation to avoid aspirative pneumonia.
4. Discussion Meningiomas arising at the foramen magnum have a slowly progressive clinical course, leading to dysesthesia, asymmetric motor weakness, gait ataxia, and, less commonly, lower cranial nerve affection. MRI consists the gold standard method for proper diagnosis and treatment planning. FMMs are known for their close relationship with important vascular, nervous and bone-articular structures. As a direct consequence, a great number of different surgical approaches have been described in the literature [4,6,7,9,23–26]. Anterior approaches, such as transoral or transcervical, are widely accepted for resection of extradural or ventrally-located tumors in the foramen magnum region [4,6,9]. The main advantage of the transoral approach is its direct route to the anterior foramen magnum. Possible complications include craniocervical instability, velopalatine insufficiency, a higher risk of postoperative cerebrospinal fluid leakage, and meningitis. In our experience, the complications far outweigh the benefits [18]. Moreover, FMM located strictly ventral to the brainstem are relatively rare, since they have often lateral extensions [23]. The transcervical retropharyngeal approach is usually favored in extradural lesions, but it is not widely used because complete resections in rostrally and laterally-extending tumors are troublesome and technically difficult [27]. Lateral approaches like the pre-sigmoid and transpetrosal include an extensive bone removal and high risk of injury to the seventh and eighth cranial nerves, especially if trans-cochlear drilling is necessary. In contrast, the posterior suboccipital midline approach is an easy and straightforward option. Vertebral arteries and cranial nerves are well manageable and, compared with the trans-oral or trans-cervical variants, the operation field is much
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Table 2 Clinical and radiological characteristics of 24 patients with FMMs. Symptom
Sign
Location size cm
Condyle removal
Vertebral artery
Remotion simpson
Postperative new deficts
Follow up
1
47y, M
Hemiparesis right, gait ataxia
Spinoclival anteriolateral right 3,6
No
Exposed and displaced
IV
45y, F
No
Exposed and displaced
II
82 months; No recurrence
3
72y, F
No
Exposed and displaced
III
No
78 months; No regrowth
4
52y, F 44y, F
Clivospinal anteriolateral right 2,8 Clivospinal Paresis upper limb left anterolateral Left 2,0 Tetraparesis, gait ataxia Clivospinal anteriolateral left 2,0 Slight IX, X cranial nerves Clivospinal deficits posterolateral right 2,2 Slight triparesis, gait ataxia Clivospinal anterior 2,5
Slight impairment of previous deficits of the hemiparesis No
94 months; No recurrence
2
Cervical pain, motor weakness, gait unsteadiness Cervical pain
No
Exposed and displaced
I
No
53 months; No recurrence
Yes, 1/3 post. Condyle
Exposed and untouched
I
Slight dysphagia
46 months; No recurrence
Yes, 1/3 post. Condyle
Exposed and displaced
II
Clivospinal posterior 2,0
No
Exposed and displaced
II
Clivospinal posterolateral right 3,3 Spinoclival anterolateral right 3,8 Clivospinal anterolateral left 2 cm Spinoclival anterolateral right 4,2
No
Exposed and displaced
I
46 months; No recurrence Slight impairment of previous deficit (transitory) Xth cranial nerve unilateral 32 months; No recurrence (transitory) No 36 months; No recurrence
No
Exposed and displaced
IV
No
30 months; No regrowth
No
Exposed and untouched
I
No
28 months; No recorrence
No
Exposed and displaced
II
No
28 months; No recorrence
Clivospinal anterolateral left 3,0
No
Exposed and displaced
II
No
20 months; No recorrence
Clivospinal lateral right 2,0 No Clivospinal lateral left 3,0 No
Exposed and displaced Exposed and displaced
II II
No Slight transient hypoglossal paresis
8 months; No regrowth 6 months; No recorrence
Spinoclival anterolateral left 1,5 Spinoclival anterolateral left 2,5 Spinoclival anterolateral left 1,5 Clivospinal anterolateral left 2,7 Clivospinal anterior 1,5 Spinoclival anterolateral left 2,8
No
Exposed and untouched
II
No
82 months; No recorrence
No
Exposed and displaced
II
No
78 months; No recorrence
No
Exposed and displaced
II
No
76 months; No recorrence
No
Exposed and untouched
II
No
73 months; No recorrence
No No
Exposed and untouched Exposed and untouched
II II
No Slight transient paresis upper left limb
72 months; No recorrence 54 months; No recorrence
No Clivospinal anterolateral right 1,7 Clivospinal lateral right 3,0 No
Exposed and displaced
IV
Slight transient dysphagia
48 months; regrowth
Exposed and untouched
II
26 months; No recorrence
Clivospinal anterior 2,0
No
Exposed and displaced
IV
Slight transient Lower motor neurone dysarthria and dysphagia No
23 months; No regrowth
Clivospinal posterior 2,6
No
Exposed and untouched
II
No
21 months; No recorrence
5
Occipital pain, vertigo, diplopia Occipital pain Occipital pain, slight dysphagia, visual disturbance Cervical pain; parasthesia upper limb, motor weakness, Cervical pain, dysphagia, gait unsteadiness Motor weakness
Slight paresis upper limb
6
61y, F
7
69F
8
74F
9
52F
10
82F
11
42F
12
64F
13 14
27y, M 46y, F
15
55y, F
Cervical pain, shouder pain, IX, X, XI, XII cranial nerves dysphagia, hoarseness deficits Cervical pain, dysphagia IX, X, XI cranial nerves deficits Hypesthesia, paresis upper Slight paresthesia upper limb right, motor limb weakness Tetraparesis, gait ataxia Cervical pain, slight dysphagia, gait unsteadiness No deficits No symptom Cervical pain, disesthesia Gait ataxia face, gait unsteadiness, urge incontinence No symptom No deficits
16
54y, M
Vertigo
17
45, M
No symptom
Slightly horizontal nystagnus No deficits
18
45, F
Cervical pain
Hypesthesia
19 20
10y, F 51y, F
21
13y, M
No symptom No deficits Hypesthesia Cervical pain, slight paresthesia upper limb left, motor weakness No symptom No deficits
22
81y, F
Occipital pain
23
51y, M
24
55y, F
Paresthesia bilateral upper Gait ataxia limbs, with predominant right, gait unseadiness No symptom No deficits
IX, X, XI cranial nerve deficit Hemiparesis right
Hypesthesia
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Patient Age/sex
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wider and not so deep. For tumors located exclusively ventral to the brainstem, the approach can be extended laterally [18]. Several lateral modifications have been described, like the far-lateral with or without transcondylar extension [3,25]. In our experience, a midline suboccipital craniotomy with no drilling of the posterior third of the occipital condyle proved to be sufficient to expose the ventral part of the foramen magnum region, with the main advantage of offering an operation field not so deep as compared with that obtained by trans-cervical, trans-oral, and even lateral approaches. The far-lateral transcondylar approach involves exposure of the transverse process of C1. However, it is more time-consuming and implies higher risks of CSF-leakage and (always) cranio-cervical instability. The far-lateral supracondylar approach, instead, is tailored to the area above the occipital condyle, and similarly permits exposition of the foramen magnum and clival areas. In special cases, neck dissection may be necessary [24]. The far-lateral approaches provide lateral exposure of the brainstem, thus permitting a safe dissection without significant retraction. The entire longitudinal and lateral extensions of the tumor, as well as eventual extra-dural components, can be achieved using this approach [25]. The main drawback is the aggressive bone removal necessary. Some variations desired to overcome this drawback, like the retrocondylar approach, involve only partial occipital condyle drilling and do not cause any craniocervical instability [28]. Posterior and posterolateral FMMs can be safely resected via a standard midline suboccipital approach. Controversy still exits, however, regarding the optimal management of ventral or ventrolateral lesions. In those cases, surgery could result in undue brainstem retraction, higher rates of subtotal resection (STR), and postoperative morbidity, due to inadequate exposure [5,29,30]. It has been suggested that patients operated on via conventional suboccipital approaches have worse clinical outcomes than patients operated on via the transcondylar route [5,9,26]. Those findings were contested by Goel et al., who reported gross-total resection (GTR) of 14 anterior or anterolateral FMMs through a conventional posterior suboccipital approach, similar to the results obtained by other authors [18,31,32]. Our experience confirmed that the midline suboccipital subtonsillar approach was accurate in safely removing anterior, anterolateral, and posterior FMMs. There was no significant postoperative complication in the remainder of the patientes, and their conditions improved after surgery.
5. Conclusion Conclusively, the subtonsillar approach provides excellent access, allowing a direct view of the foramen of Luschka laterally and up to the middle cerebellar peduncle [33]. In addition, the STA takes into consideration the anatomical displacement commonly caused by the lesion, providing a direct route to the same. Radical resection of the lesion – even of its extra-cranial parts – is feasible and safe with a standard craniotomy, which does not require additional time for bone drilling. Moreover, extradural problems can be avoided, such as dealing with the jugular bulb or with the jugular foramen. The STA is limited, however, in tumors extending too far inferiorly. In these cases, additional neck dissection is usually advisable [20].
Declaration of interest The authors state that they have no conflicts of interest to disclose. The authors alone are responsible for the content and writing of the paper, and have all agreed with its content.
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Acknowledgments The authors would like to thank the research funding agencies CAPES Brazil for the financial support with a research scholarship.
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