Foramen Magnum Meningioma
Keywords: foramen magnum meningiomas, far lateral approach, extreme lateral approach, occipital condyle, vertebral artery, surgical resection, operative approach
Foramen magnum (FM) meningiomas are rare overall, yet relatively common specific to that region. These are slow growing tumors and therefore present late in the course due to involvement of adjacent brainstem and lower cranial nerves. Surgical resection provides the best chance for cure but is challenging due to its critical location. A detailed anatomical knowledge of bony anatomy around the FM, lower eight cranial nerves, and vertebral artery (VA) is essential for a safe surgical approach. The tumor location in relation to the brainstem dictates the surgical approach and is the main determinant for surgical difficulty and morbidity. Tumors located posterior and posterolateral to the brainstem are easily approached through a suboccipital approach. However, tumors ventral to the brainstem require complex surgical approaches including far-lateral approach or extreme lateral approach. The critical steps involved in these approaches are the occipital condylar resection and mobilization of the VA. However, majority of the FM meningiomas can be safely removed without the condylar resection, due to the significant brainstem shifting associated with these lesions. With the use of neuronavigation and neuromonitoring, the rate of complete resection has been reported to be more than 85%, with an acceptable recurrence rate of 0 to 12%. Gamma knife radiosurgery has emerged as a useful adjunct to surgery and has a promising role in complex and large tumors especially after subtotal resections.
The foramen magnum (FM) region is a highly complex territory of the skull base and contains many important and vital structures. Meningiomas in this region though rare as compared to other intracranial locations, comprise more than three-fourth of the tumors. 1, 2 Close proximity to the highly sensitive structures like medulla and lower cranial nerves poses formidable challenge in their surgical resection. The difficulty increases multifold especially in anteriorly located lesions which are anatomically hidden from the surgeon’s view. Many new surgical approaches and modifications have been developed and compared to provide adequate access to deal with these lesions. With recent improvements in surgical techniques and image guidance, almost all lesions are now surgically resectable with acceptable complications.
The earliest description of a meningioma at the FM region was in 1872 by Hallopeau, he described his autopsy finding of a patient who died within 5 months of developing motor symptoms. 3 Surgery around this region was considered intimidating and less rewarding. Later, in 1922, Fraizier published his series of 14 patients of spinal cord tumors which included one FM meningioma. 4 He described his difficulty in achieving a total resection in a patient with a craniospinal tumor in which two-third of the tumor was intracranial. He described “…had it not been for the fact that the respiratory act was sustained alone by the half of the diaphragm, its removal could have been accomplished.” Unfortunately, the patient developed respiratory arrest during the operation and died. Three years later, in 1925, Elsberg and Strauss could achieve the successful removal of a FM tumor in which the patient had a complete symptomatic improvement. 5 Literature on FM meningioma was sparse in the mid twentieth century and most of the cases have been described along with other spinal cord or intracranial tumors. Management of FM meningioma as a separate entity was discerned and described by Yasargil, who documented his series of 114 cases in 1980. 6 Subsequently, Bernard George and colleagues presented their series of 230 FM region tumors at 44th Annual Congress at Brussels in 1993, which contained 106 cases of meningioma. 7 Most of the patients in the early literature were operated by the classic posterolateral approach with variable degree of resection rate. The resection rates were less appealing for the anterior FM meningiomas. Subsequently, Heros described the feasibility of far lateral approach which revolutionized the surgical approaches to the FM region. 8 Since then, various modifications and nuances have been described and compared to increase the resectability of the tumors while reducing the complication rates.
14.3 Surgical Anatomy
On account of the invaluable contribution by Albert Rhoton, the microsurgical anatomy of the FM region has become more lucid for neurosurgeons. 9 The intricate anatomy at this location has been of great interest to neuroanatomist and multiple reports have been published on cadaveric dissections. Similarly, in quest of defining the optimal approach, various quantitative anatomical studies have been described, focusing on different skull base approaches and their modifications. 10, 11, 12, 13, 14, 15, 16, 17 With respect to approaches for the FM meningiomas, it is important to understand the microsurgical anatomy of three basic yet most important structures in this region which include the occipital condyles, vertebral artery (VA), and the cranial nerves of the posterior fossa.
14.3.1 Occipital Condyle
The FM is ovoid in shape in its anterior posterior direction and occipital condyles occupy its anterior half. The occipital condyles face downward, anteriorly, and laterally, and slightly bulge into the foramen. It is attached to the superior facets of the atlas and forms the occipito-atlantal joint. The condylar fossa is a depression on the occipital bone that lies just above and posterior to the posterior lip of condyles. The condylar fossa contains the condylar vein which connects the vertebral venous plexus to the sigmoid sinus. The condylar fossa is the main bony structure that is removed during a far lateral approach that provides a great degree of intradural exposure. The occipital condyles are bean-shaped and for anatomical description have been divided into three thirds. The most important structure important in relation to the condyles is the hypoglossal nerve that runs in the hypoglossal canal which lies above the mid-third of the condyle. The hypoglossal nerve traverses anterolaterally at an angle of 45° to the sagittal plane after arising from the brainstem and is relatively fixed. During condylar resection, the safe limit (considered as the resection of medial one-third of condyle) is defined by the exposure of cortical bone over the hypoglossal canal. Other bony structures that are relevant to this area are the jugular process and jugular tubercle but are less commonly removed in meningioma resection.
14.3.2 Vertebral artery
Detailed knowledge of the VA anatomy especially on its extradural course is of paramount importance during surgical approaches of the FM. The artery is less obvious in this region and due to its variable and complex course, it is more prone for injury during soft tissue dissection. During a routine far lateral approach, the VA is usually exposed from the transverse foramen of C2 to its intradural course (▶ Fig. 14.1a). The artery traverses vertically and slightly laterally from the transverse foramen of C2 to transverse foramen of C1. After exiting from C1 foramina, the artery curves medially and posteriorly around the atlanto-occipital joint. During this course, it rests on the superior surface of posterior arch of atlas called as the vertebral groove, which often gets ossified to form a canal. After exiting medially from the groove, the artery turns anteriorly and medially to pierce the dura. During its dural entry, a cuff of dura around the artery may form a sleeve which is an important anatomical point to realize during the dural incision. The artery gives rise to many meningeal branches during its extradural course. The posterior spinal artery and possibly the posterior inferior cerebellar arteries are important branches during its dural entry and should always be searched for during dissection around this region. The VA may need to be mobilized during the course of surgery to expose the atlanto-occipital joint. The V2 segment is usually freed up by drilling the posterior ramus of transverse foramina of C1 which along with dissection from the vertebral groove allows the artery to be mobilized inferomedially. The extradural course of the VA, especially in its third segment, is surrounded by a vertebral venous plexus which can be a source of brisk bleeding while dissecting the VA. Therefore, a subperiosteal dissection is always advisable that avoids entry into the periarterial soft tissue containing the plexus. The intradural course of the VA is variable with formation of loops and curves while resting on anterior clival dura. After coursing anteromedially, it joins the opposite VA to form the basilar artery (BA) which usually lies at the pontomedullary junction. The posteroinferior cerebellar artery is an important branch from this segment of VA.
Fig. 14.1 (a) Illustration showing the course and bony relations of the V2 and V3 segment of vertebral artery (VA). (b) Illustrations showing intracranial exposure after dural opening in far lateral approach. Note the course of the lower cranial nerves and the intracranial VA. (c) Schematic diagram showing various skull base approaches to foramen magnum region. Note that with subsequent lateral extension of the bony resection, the exposure to the contralateral side of anterior foramen magnum is getting increased. (d) Illustration showing the hockey stick skin incision in far lateral approach.
After the dural opening, the dentate ligaments serve as the midline structure that divides the spinal canal into anterior and posterior compartments. The rootlets of C2, C1, and the spinal part of accessory nerve are the main neural structures found in the upper spinal canal. The first cervical nerve runs just below and posterior to the dural entry point of VA. Above this level are the important lower cranial nerves which run anterolaterally after origin from the brainstem (▶ Fig. 14.1b). The glossopharyngeal nerve arises as one or two rootlets, the vagus as series of seven or more rootlets and the cranial accessory as four to five rootlets and all of them form a fan-like structure running across the jugular tubercle into the jugular foramen. In most of the cases, the lower cranial nerves are displaced either anteroinferiorly or posterosuperiorly depending upon the origin of the tumor (described later). The hypoglossal nerve runs behind the VA into the hypoglossal canal after its origin from the medulla.
14.4 Epidemiology, Clinical Presentation, and Imaging
FM meningiomas are rare and only comprise about 0.3 to 3.2% of all meningiomas. 18 However, when compared to all posterior fossa pathologies, it accounts for a sizable proportion of all tumors. More specifically, in the FM region, this is the most common pathology encountered and comprises about 70% of the lesions. 19 Similarly, among spinal meningiomas, around 8.6% of the lesions are located in the FM region extending to the upper cervical spine. Most of the patients present in their fourth to sixth decade. However, pediatric patients have also been reported harboring FM meningiomas. Athanasiou et al in their literature review of 34 pediatric patients with FM meningiomas found that, the mean age of presentation is less (9.95 years) as compared to meningiomas at other locations (14–15 years) and attributed this to early development of increased intracranial pressure, brainstem compression and hydrocephalus inherent to its location. 20 Most of the FM meningiomas in the pediatric age group or at multiple locations are associated with neurofibromatosis type 2 (NF-2). 21 Similar to meningiomas at other locations, FM meningiomas are more common in female with male to female ratio of 2–4:1.
Meningiomas in the FM region are particularly slow growing and therefore present very late in the course of the disease. 22 Most of the symptoms are due to chronic compression brainstem and spinal cord and occasionally the cranial or spinal nerves. The symptoms are initially vague and nonspecific that leads to initial misdiagnosis to cervical spondylotic myelopathy, cervical disk herniation, multiple sclerosis or other noncompressive myelopathy. 19 The diagnostic delay from the onset of symptoms was higher in older literatures that was as high as 6.5 years, 23, 24 however, recent studies report an average delay of almost 30 months. 18 In a significant subset of patients, the lesion is totally asymptomatic and is detected during routine imaging for head trauma or other nonrelated causes. In symptomatic patients, the most common presentation is cervical pain and headache. The headache is related to the stretching of the cervical and posterior fossa dura. In few patients, the headache is progressive and is due to increased intracranial pressure secondary to hydrocephalus. The hydrocephalus is due to the obstruction of the CSF pathway from brainstem compression and usually does not need permanent CSF diversion. However, it is important to clinically differentiate the headaches due to raised intracranial pressure from other causes, which needs urgent intervention. The most common neurological manifestation due to brainstem compression is the gait ataxia followed by spastic quadriparesis. Typical patterns though not seen in all cases are the cruciate paresis and rotating palsy. In the former pattern, ipsilateral arm is involved followed by contralateral leg, contralateral arm, and ipsilateral leg, respectively. Rotating palsy involves extremities in a rotating sequential pattern from ipsilateral arm to ipsilateral leg, contralateral leg and then to contralateral arm. In tumors with significant caudal extension to the cervical spine, lower motor involvement is seen leading to atrophy of muscles of arm, forearm, or even of the intrinsic muscles of hands. Sensory involvement is not very common but is possible in larger tumors with significant compressions where features of dissociated sensory loss or a Brown-Sequard syndrome are seen. In tumors with more cranial extension, cranial nerves and cerebellar peduncles or hemispheres are likely to get compressed. The most common involvement is of the spinal accessory nerve which gives rise to atrophy of the trapezius and sternocleidomastoid muscles. Other infrequently involved nerves are the hypoglossal nerve leading to tongue atrophy and lower cranial nerves that gives rise to dysphagia or dysphonia. More proximal cranial nerves like vestibulocochlear, facial, or trigeminal nerves are very rarely involved. Cerebellar symptoms are mostly bilateral due to peduncular involvement or compression of crossing fibers in the brainstem. Unilateral appendicular ataxia is possible in laterally located tumors due to compression of cerebellar hemispheres.
The formal imaging studies required for these tumors are the nonenhanced computed tomogram including the bone windows and MRI with gadolinium. Imaging is very crucial in surgical planning and intraoperative navigation. Similar to meningiomas at other locations, these tumors are iso- to hypointense on T1, iso- to hyperintense on T2, and enhance brightly with gadolinium. The T2 hyperintensity is related to the tumor water content and softer and friable tumors appear brighter in this sequence. There is little confusion in getting a diagnosis of meningioma with presence of these typical imaging features. However, in few patients with atypical imaging findings other differential diagnoses of intradural and extradural tumors at FM meningiomas should be excluded. The sagittal and coronal images are important to define the tumor extension and surgical planning. Other important features to be looked in the imaging are the course of the VA, degree of compression, and shifting of the brainstem. CT scans are invaluable mostly to delineate the cranial anatomy especially the occipital condyle, jugular tubercle, hypoglossal foramen, etc. In some cases, tumors are associated with calcifications which is easily detected by the CT scan. Angiograms like CT or MR are rarely necessary unless a detailed vascular anatomy needs to be studied. Such situations arise in patients with suspected VA encasement or invasion. Secondly, when a more lateral approach is planned a CT angiography is helpful to show the extracranial course of VA and to rule out any anomalous course or branch on the side of approach.
14.5 Classification of Foramen Magnum Meningioma
There have been several classification schemes for FM meningiomas all of which are centered on the description of tumor with respect to the tumor position in relation to the brainstem. The earliest classification put forward by Cushing and Eisenhard describe tumors based on their vertical extensions. 25 The “craniospinal meningiomas” comprised tumors arising from the dura over the clivus ventral to the brainstem with possible extension to upper spinal canal. The other variant “spinocranial meningiomas” comprised tumors arising from the spinal dura posterior to the spinal cord with possible intracranial extension dorsal and lateral to medulla. George and Lot 18 described tumors based on their position in a horizontal relation to the brainstem. They classified tumors into posterior, lateral, or ventral variants. Bruneau and George 26 included the relation of tumor to VA into their classification system and described four tumor types: type-A tumors arise below the VA and grow upwards, type-B tumors arise above the VA and grow downwards, and type-C tumors are described by the vertebral artery coursing across the lesion with or without encasement. The C1 type is intradural whereas C2 type has dural penetration with an extradural component. The origin of the tumor in relation the VA is important in two possible ways. Firstly, tumors originating from below the VA pushes the lower cranial nerves upward and posteriorly putting the surgeon in an advantageous position. However, tumors arising from above the VA pushes the nerves anteriorly and inferiorly and thereby are encountered early in the course and requires careful dissection. Secondly, it is important to estimate the involvement of the VA by the tumor. In most patients, encasement of the artery by intradural tumors are less problematic because of the presence of a well-preserved arachnoid plane between the tumor and artery. However, extradural tumors arising from the spinal dura can involve the extradural part of the vertebral artery. In such cases, tumors may involve the adventitia of the artery, thereby making surgical excision difficult.
Despite many proposed classifications, most of the surgeons group their cases into two types, i.e., the ventral type and posterolateral type. 22 This simplest categorization does have clinical utility while considering appropriate surgical approach. The vertical extension of the tumor has got a lesser contribution in choosing the right approach.
14.6 Operative Approaches
An important hindrance to all skull base approaches dedicated to this area is the significant high rate of intraoperative complications and postoperative morbidity. However, with better understanding of the anatomy, use of intraoperative monitoring, and intraoperative navigation tools there has been significant decrease in intraoperative adverse events with a resulting improved postoperative outcome. In addition, with advent of stereotactic radiosurgery, there has been a trend towards more conservative surgical resection. However still, many skull base surgeons are proponents of gross total resection in the index surgery itself as it gives the best chance of cure. With experienced hands, even complex tumors could be resected completely, with acceptable morbidity.
The primary determinant for a particular surgical approach over others is the location of the tumor in the horizontal axis with respect to midline. Generally, tumors located posterior and posterolateral to brainstem are easy to access from a posterior route. Tumors ventral to the brainstem are difficult to approach from a posterior perspective because of the brainstem and therefore requires more lateral approach. Overall, the surgical approaches to the FM meningiomas are divided into three types with various possible modifications. These approaches with progressively increased complexity and morbidity includes the posterior suboccipital approach, far lateral approach, and extreme lateral approach (▶ Fig. 14.1c). Ventral approaches like open transoral or endoscopic approaches have been described historically but rarely used nowadays.
14.6.1 Posterior Suboccipital Approach
This is the simplest and frequently used approach for posterior and posterolateral tumors in which the main bulk of the tumor displaces the brainstem anteriorly. The cranial nerves and the spinal nerves are displaced anteriorly and superiorly and therefore pose little risk while dissection. This approach is feasible even in more anteriorly located tumors because of the brainstem shift associated with most of the tumors. 27, 28
The patient is positioned in prone with the head slightly flexed to expand the suboccipital space. A skin incision is placed in the midline starting from just below the inion upto the spine of the third cervical vertebra. The skin incision is deepened and the posterior rim of the FM and posterior arch of atlas and axis are identified. The muscles are dissected laterally up to the condylar fossa. A sub-occipital craniotomy is done including removal of posterior arch of atlas. In pure sub-occipital approach, identification of the vertebral artery is usually not required, however, its location should be confirmed to avoid its inadvertent injury. The tumor is usually identified just after the opening of the dura. In posteriorly located tumors, all the spinal nerves and the denticulate ligament are displaced anteriorly and visualized after removal of the tumor. In few patients, the tumor has both anterior and posterior components. In such cases, the anterior component (identified as tumors located anterior to denticulate ligament) can be removed by working in between the nerve rootlets. The C1 and C2 nerve rootlets can be sacrificed safely in case it is required for resection. After removal of the tumor, the dural attachment is coagulated and the thecal sac is closed.
14.6.2 Far Lateral Approach
This is essentially the lateral extension of the suboccipital approach. The far lateral approach was popularized by Heros in the late twentieth century. 29 Various modifications have been introduced to the original description, however, the basic principle involves removal of the lateral rim of the FM towards the condylar fossa along with the part of C1 posterior arch which provides a more inferolateral view to the midclivus without need of brainstem retraction. Need of condyle resection is the most controversial topic in this approach, however, in particular to the FM meningiomas, most of the surgeons agree that condyle resection is not really necessary for the removal of ventral meningiomas. 27, 30, 31, 32, 33, 34, 35
For a far lateral approach, multiple patient positions have been described including lateral, park bench, and sitting positions. Lateral and park bench positions are mostly used based on surgeon’s preference. Sitting positions are preferred by few surgeons as it provides a more anatomical view along with a blood less field. However, complications inherent to sitting positions like air embolism and deep vein thrombosis, makes it less favorable. Irrespective of the position used, it is important to avoid gross manipulation of the craniovertebral junction, especially head flexion, as it may compromise the brainstem which is already compressed by the tumor. Intraoperative monitoring helps identifying any adverse event related to brainstem compression both during positioning and surgery. Most of the surgeons prefer an inverted J-shaped incision with the horizontal arm lying in the midline and the horizontal arm curving below the inion laterally up to the base of mastoid. Alternatively, a curvilinear lazy S incision similar to the incision used for retrosigmoid approaches can also be used, which is also the authors’ preferred incision (▶ Fig. 14.1d). After careful soft tissue and muscle dissection, the FM is exposed laterally up to the medial border of the condylar fossa. Similarly, the posterior arch of atlas (and the axis in cases) is exposed laterally up to the tip of the lateral mass. The VA is carefully identified along the upper border of the C1 arch when it curves posteriorly after arising from the C1 foramen. In some cases, the VA groove on the upper surface of C1 arch is ossified and converted into a canal. In such cases, it is very difficult to mobilize the VA and requires careful drilling of the canal. Significant venous bleeding from perivertebral venous plexus is a possible complication during dissection of VA. Therefore, it is advisable to develop a subperiosteal dissection without violating the periarterial soft tissue sheath. Mobilization of the VA from the C1 groove is enough in most of the cases, however, some cases may require more lateral approach and needs complete mobilization of the vertebral artery from the C1 foramen. In such cases, the foramen can be opened with drilling of the posterior ramus. A subperiosteal dissection usually takes the artery out of the foramen. Excision of the lateral mass of the C1 can be done if required for a more lateral exposure and to provide more surgical freedom. This medial transposition of the VA gives more exposure and improves the surgical freedom. Though not considered as a routine in far lateral exposures, medial transposition of the VA is considered essential for extreme lateral approaches. Another important consideration at this point is to identify any possible developmental anomaly of the VA or presence of any aberrant course.
A suboccipital craniotomy is performed similar to standard retrosigmoid approach exposing the junction of the sigmoid and transverse sinuses. However, a more caudal and lateral craniotomy is added by removing the condylar fossa, which is the main bony structure that needs to be removed to achieve a significant lateral exposure. Often termed as “condylar fossa approach”, this technique actually gives a significant preliminary exposure to the petroclival region and midclivus. 15 The condylar fossa contains the condylar vein in its depth which is a tributary of sigmoid sinus and can be easily controlled with coagulation. However, in some patients, the condylar vein is of significant size and needs careful control. Just lateral to the condylar fossa lies the occipital condyle. The occipital condyle is an important landmark in the far lateral approach and is subject to many controversies regarding its need of removal. From an anatomic point of view, occipital condyles occupy the anterolateral quadrant of the FM and should obstruct view of the midclivus while looking from a posterolateral aspect. However, in FM meningiomas, because of significant amount of brain shift, an unrestricted view to the anterior FM can be easily obtained, even in the presence of the condyles (▶ Fig. 14.2 a and b). Many anatomical studies have been carried out to define the significance of condyles in far lateral approaches. 13, 36, 37 In a subset of patients in whom the occipital condyles are prominent and significantly bulge into the FM can become problematic and can hide a significant proportion of the tumor, even in the presence of brain shift. These factors should be taken into consideration during presurgical planning, and therefore needs careful observation of the bony anatomy in preoperative CT scans. When there is a need of condylar resection, the VA should be carefully mobilized and its dural entry point is ensured. The joint capsule is identified and opened. The posterior lips of the occipital condyles are carefully drilled. The important landmark to the limit of posterior one-third of occipital condyle resection is the hypoglossal canal. The bone can be drilled till cortical bone lining of the hypoglossal canal is reached which is considered to be the maximal safe limit. The orientation of the intradural part of hypoglossal nerve should be observed to avoid injury. The lateral extension to the craniotomy can be obtained by doing a more supracondylar drilling which can reach up to the jugular tubercle. By this time, a sufficient exposure of the anterior aspect of medulla and pons is usually obtained to safely perform tumor resection, even in purely ventral tumors with contralateral extension. After sufficient bony work, the dura is opened parallel to the sigmoid sinus that curves around the cuff of VA and extends down to the cervical dura. With lateral retraction of the dura and rostromedial retraction of the cerebellum, the whole of the anterolateral cisterns around the brainstem including the mid and lower clivus can be visualized. At this point, the cranial nerves serve as the main obstacle for dissection. The trigeminal nerve and the VII-VIII nerve complex lie anterolaterally and the lower cranial nerves lie laterally forming a transverse neural barrier. For this reason, the anterior dissection and tumor removal should proceed working in the corridors between the nerves. For posteriorly located tumors, it hardly ever creates problem, because the nerve complex are shifted anteriorly and are seen beneath the arachnoid later in the course. Even with an excellent exposure it is possible to miss some part of the tumor that lies to the contralateral side behind the brainstem because of obstructing line of vision. Therefore, for FM meningiomas with significant contralateral extension, it is important to access the completeness of the tumor removal by looking towards these blind points.
Fig. 14.2 Intraoperative images (a) Exposure after far lateral approach showing the tumor in the ventral foramen of magnum, posterior inferior cerebellar artery and the lower cranial nerves. (b) Image after complete resection of the tumor. (c) Intraoperative images in a craniospinal tumor in the anterolateral location showing relation of the tumor to the lower cranial nerves and the C1 nerve root (d) Image after complete resection of the tumor.