Surgical Management of Tumors of the Foramen Magnum

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Chapter 43 Surgical Management of Tumors of the Foramen Magnum

Jose Alberto Landeiro, Roberto Leal Silveira, Cassius Vinícius Corrêa Dos Reis

The foramen magnum (FM) comprises a bony channel formed anteriorly by the lower third of the clivus, the anterior arch of the atlas, and the odontoid process. The lateral limits are the jugular tubercle (JT), the occipital condyle (OC), and the lateral mass of the atlas. Lastly, the FM is limited posteriorly by the lower part of the occipital bone, the posterior arch of the atlas, and the two first intervertebral spaces.¹^–³

The FM encloses the vertebral arteries (VAs) and their meningeal branches, the anterior and posterior spinal arteries, the lower cranial nerves (IX, X, and XI), and the roots of the C1 and C2 vertebrae. The neural structures located at the FM are the cervicomedullary junction, the cerebellar tonsils, the inferior vermis, and the fourth ventricle.¹^–³ It is surrounded by veins, venous sinuses, and the jugular bulb. Hence, when approaching this region, surgeons must avoid manipulation and retraction of those neurovascular structures and, consequently, preserve anatomy and function.

There is a broad spectrum of intra- and extradural surgical pathologies of the FM. Tumors represent almost 5% of spinal and 1% of intracranial neoplasms,¹ which consist mostly of meningiomas, neurinomas, and chordomas.¹^–⁵

In the past, these lesions were approached posteriorly and eventually via the transoral route; however, the results of these techniques were disappointing.⁶ The introduction of computed tomography (CT) scan and magnetic resonance imaging (MRI) allowed the improvement of anatomic knowledge and the development of microsurgical techniques and skull base approaches. Therefore, treatment of these tumors has evolved and remarkable improvement in surgical results has been achieved. Nevertheless, despite these advances, surgery of FM tumors is still associated with a high rate of morbidity.

Clinical Presentation

The clinical presentation associated with FM tumors is insidious. Because of their slow-growing pattern, their indolent behavior, and the wide subarachnoid space at this level, the mean length of symptoms before diagnosis is 30.8 months.^3,⁷ In early stages, patients complain of occipital headache and cervical pain. This pain is described as deep and is aggravated by neck motion, coughing, and straining. As the tumor grows, sensory and motor deficits develop. The classic syndrome of FM tumors, mainly of meningiomas placed anteriorly, is an asymmetrical deficit defined by weakness, paresthesis, and spasticity, first in the ipsilateral arm and progressing to the ipsilateral leg, then to the contralateral leg, and finally to the contralateral arm. Long tract signs characteristic of upper-motor lesions are the presence of atrophy in the intrinsic muscles of the hands. Later findings include spastic quadriparesis, respiratory dysfunction, and lower cranial nerve deficits.^6,⁷ In extradural tumors, especially in cranial base chordomas, diplopia is the symptom most commonly reported and headache is the second-most-common symptom.⁵

Classification of the Tumors

Tumors of the FM are classified according to their origin. They can arise in the FM itself or secondarily from surrounding areas. Most classifications focus on meningiomas and usually do not regard bone tumors. Among the many classifications of meningiomas of the FM,⁶^–⁸ the one most frequently used by neurosurgeons is the classification from Bruneau and George.³ The main objective of this system is to define the surgical strategy preoperatively. Based on this classification, meningiomas of the FM are classified as intradural, extradural, or intra- and extradural. According to their insertion on the dura, meningiomas are anterior if insertion happens on both sides of the anterior midline, anterolateral if insertion occurs between the midline and the dentate ligament, or posterior if insertion is posterior to the dentate ligament. The other landmark used for classification is the relation to the VAs, because meningiomas of the FM can develop above, below, or on both sides of the VAs. Intradural meningiomas are the most common type, and most of them arise anterolaterally;⁴^–⁸ these are followed in frequency by posterolateral tumors. Tumors that arise purely posteriorly and anteriorly are rare.⁷

The surgical approach to extradural tumors is based on their relationship with the C1 lateral mass, OC, clivus, intradural extension, cavernous sinus, jugular foramen, retropharynge, VAs, and carotid artery. Although there are various kinds of tumors, they present a similar surgical aspect. A position in front of, or lateral to, the cervicomedullary junction; a closer relationship with the VAs and their branches; lower cranial nerves; and complex articulation between the occipital bone and the C1 and C2 vertebrae are some of these surgical aspects. The size, position, and nature of the tumors define the surgical approach and steps, such as drilling the lateral wall of the FM and transposing the VAs. The definition of the space between the cervicomedullary junction and the lateral wall of the FM, the so-called surgical corridor,⁷ is also an important consideration. Large tumors, either anterior or anterolateral, push the cervicomedullary junction posteriorly, creating a surgical avenue for tumor removal. In contrast, small tumors and an elongated FM may require additional space, which can be obtained via the condyle or the lateral mass of C1, with transposition of the VAs.⁵

Preoperative Imaging

The preoperative workup includes MRI and CT scan. With the availability of CT angiography and magnetic resonance angiography, conventional angiography is rarely indicated unless embolization is planned in highly vascularized tumors. Preoperative imaging studies allow for planning of the surgery; for this, the following information must be retrieved from the images: the nature of the tumor (intra- and/or extradural), its location and attachment, its relationship with the cervicomedullary junction, its caudal and rostral extension, the position and possible involvement of the VAs and their branches, the shape of the FM, the dominance of the VAs, the venous drainage patterns and dominance, and bony involvement. T1-weighted MRI with contrast enhancement clearly defines the tumor and the dural attachment site and discriminates between the tumor and the brain stem. T2-weighted MRI provides information on the arachnoid plane between the tumor and the cervicomedullary junction. CT using sagittal, coronal, and axial viewing and bone window remains the tool of choice for the study of bone involvement, the shape of the FM, and the surgical corridor.¹^–³ ^,6 ^,7

Choosing the Best Approach

The principal factors that determine access to the lesions placed at the craniovertebral junction are the nature, position, and size of the tumors and the shape of the FM.⁵ Tumors located posteriorly or posterolaterally to the cervicomedullary junction can be approached from the posterior midline, which allows an extensive sagittal view from the skull base to the entire cervical spine; however, this approach does not work well for tumors located anterolaterally. This midline route does not allow control of the VAs when the bone needs to be removed ventrolaterally. Anterior approaches via transcervical or transoral routes have been used but are not accepted widely. The transoral approach is essentially a midline and extradural approach to the inferior clivus and upper cervical spine that, combined with maxillotomy or labiomandibulotomy and glossotomy, can provide access from the superior clivus to the middle cervical spine. Nevertheless, this approach is limited laterally from both carotid arteries and VAs at the clival and spinal levels. Removal of an intradural pathology carries a high risk of cerebrospinal fluid (CSF) leakage. The dura is difficult to repair, because it comprises a limited amount of soft tissue and the subarachnoid space is exposed to the contaminated field.⁹ Anterior approaches are suitable for small extradural and bony lesions without VAs and carotid artery involvement.^4,^6,^7,¹⁰

However, minimization of the cervicomedullary retraction and of risk of CSF leakage, a firm watertight closure, and management of the OC and of the VAs are the main factors considered when choosing the approach. Among the approaches available to the FM, the so-called far lateral approach, the extreme transcondylar approach, and its variants of the lateral suboccipital approach meet these criteria. These approaches can be combined with petrosal, retrosigmoid, transtuberculum, transfacetal, and infratemporal approaches, according to the rostrocaudal extension and nature of the tumor.^6,¹¹

Extradural tumors located frontal to the cervicomedullary junction that present with or without involvement of the VAs and the lower cranial nerves, that invade the dura, and that invade and/or destroy the OC and the articulation among OC, C1, and C2 can be approached via the same route; however, these tumors often require combined approaches.^6,⁹^–¹¹

Far Lateral Approach

Positioning

Surgical results depend on the positioning of the patient. Malpositioning may result in a narrow microsurgical view, cerebral edema, increased bleeding because of impairment of venous return, and lesions of the eye, peripheral nerves, and spinal cord.¹² At our institution, we adopt the three quarter–prone position to perform lateral approaches.⁶ The side of the approach is ipsilateral to the lesion. If the lesion is placed midline, the side of the approach is usually the side of the nondominant VAs and the nondominant jugular bulb. The body is placed in a lateral position, falling to the side of the craniotomy, and the arm contralateral to the operating side is placed out of the operating table and toward the floor and is padded with an axillary roll to avoid peripheral nerve damage. The knees and other pressure points are also padded to avoid damage to the peripheral nerves, and the legs are flexed to protect the femoral nerves. To avoid displacement of the patient’s body during operating table movements, adhesive tape is attached to the operating table and then applied at the hip and shoulder. The position of the head is crucial, as the surgeon needs good exposure of the occipitocervical region for a good angle of view of the contents of the posterior fossa. A three-point head holder is placed so that the mastoid bone is at the highest point of the approach. The neck should be slightly flexed and the vertex angled down, up to 30 degrees, with the face rotated slightly ventrally. The head should not be flexed more than two to three fingers from the thyroid and should not be rotated more than 45 degrees to prevent impairment of venous drainage. The results of this positioning are the cerebellum falling away from the operating field and the contents of the lateral aspect of the FM and posterior fossa being placed right under the surgeon’s view. Intraoperative monitoring is composed of somatosensory evoked potentials, auditory evoked responses, facial nerve monitoring, and monitoring of the X, XI, and XII cranial nerves, although their use is based on surgeon preference and acceptance.^4,^5,^7,¹⁰

Skin Incision and Muscular Dissection

An inverted hockey stick–shaped incision is made, as it provides good exposure of the muscular layers, brings the surgeon closer to the surgical field, and requires lesser retraction of the soft tissues of the head and neck. A linear incision can also be used. The incision starts at the midline of the neck 5 cm below the inion and extends superiorly toward this reference. At the level of the inion, the incision is moved laterally right above the superior nuchal line and ends at the top level of the ear, about 2 to 3 cm medial to the pinna in the sagittal plane. From the last point, the incision extends down toward the mastoid and straight down over the posterior border of the sternocleidomastoid muscle. Knowledge of the muscular layers and of the neurovascular structures of the posterior neck is essential for the performance of the posterolateral approach and its variants. Dissection of each muscle is not recommended, as it creates extra dead space, increases the risk of infection, and causes muscle ischemia, which leads to wound dehiscence. We can summarize the muscular stage in three main steps: (1) elevation of the superficial muscles to expose the suboccipital triangle, (2) dissection of the suboccipital triangle to expose the VAs, and (3) transposition of the VAs if needed. At our institution, we avoid the use of cauterization to dissect the musculature, as it can damage the VAs with an abnormal loop out of the suboccipital triangle and disrupt the boundaries of the muscular layers, which damage the venous plexuses of the posterior neck, increasing bleeding and the risk of air embolism.

The skin flap is usually composed of the incised skin and galea, which are first elevated to expose the underlying pericranium. This structure, in addition to the superficial fascia of the neck, is elevated to expose the musculature of the posterior neck. The pericranium should be preserved to make a fascial graft for dural closure at the end of the operation. The first muscular layer that is exposed using this maneuver is composed by the sternocleidomastoid and trapezius muscles. They are incised near their insertion at the superior nuchal line and mastoid, leaving a cuff of tissue that is used later for closure of the incision. The underlying muscular layer (second or middle layer) is composed by the splenius capitis, longissimus capitis, and semispinalis capitis muscles. They are also incised and reflected as a single layer to expose the third layer, which forms the suboccipital triangle. The triangle is formed medially by the rectus capitis posterior major muscle, inferiorly by the inferior oblique muscle, and superolaterally by the superior oblique muscle; the VAs and its venous plexus are located in its center. Anatomic knowledge of the suboccipital triangle muscles and their insertions is essential to provide the best and safest exposure of the VAs. The rectus capitis major muscle inserts onto the inferior nuchal line and the spinous process of C2 and should be detached from the inferior nuchal line and reflected posteriorly. The inferior oblique muscle inserts onto the transverse process of C1 and onto the spinous process of C2 and the superior oblique muscle inserts at the inferior nuchal line and onto the transverse process of C1. Both muscles should be detached from the transverse process of C1 and reflected posteriorly. This maneuver exposes the C1 lamina, the VAs, the VAs venous plexus, and the C1 root.¹³

Knowledge of the muscular layers of the posterior neck is useful to prevent bleeding from the vascular structures of this region. Each muscular layer covers a vascular layer composed by a venous plexus and muscular arterial branches. Arterial blood supply for the muscles is provided by the occipital artery and by the muscular branches of the VAs. As the muscular branches of the VAs pass through the suboccipital triangle to reach the muscles, this is a crucial point for homeostasis. The main source of bleeding and air embolism in this region is the venous network. The venous system of the posterior neck is divided into two connected plexuses: (1) the suboccipital venous plexus and (2) the plexus around the VAs. The suboccipital venous plexus is superficial and is located in a space formed by the splenius capitis muscle superiorly and the longissimus capitis semispinalis capitis muscles inferiorly. The suboccipital plexus reaches the suboccipital triangle via the muscular cleft between the latter muscles and drains it into the plexus, thus surrounding the VAs through the anterior vertebral vein.¹⁴ Using the scalpel blade to cut through the muscles allows easier identification of these vascular layers and enables coagulation before bleeding and air embolism to occur.

Exposure of the Extradural VAs

The VAs is divided into four segments. V1 is the segment that runs from the origin of the artery at the subclavian artery and ends at the vertebral foramen of C6. V2 runs within the vertebral foramina from C6 through C1. V3, which is the horizontal segment of the vessel, begins at the transverse foramen of the atlas, runs through a groove on the upper surface of the posterior arch of the atlas, and ends by piercing the dura of the posterior fossa, medial and to the right of the OC. V4 is the intradural segment of the VAs and joins the opposite side vessel to form the basilar artery ¹³ (Fig. 43-1).

FIGURE 43-1 A, Muscular layers of the posterior neck dissected in a cadaver specimen. B, Venous plexus of the posterior neck. C, Segments of the VAs and their relation to the OC and the arch of C1. LCM, longissimus capitis muscle; SCM, semispinalis capitis muscle; SOVT, suboccipital venous plexus; SOT, suboccipital triangle; Cond., occipital condyle.

Exposure and transposition of the VAs is not needed in the basic far lateral approach, in which drilling of the OC is not required.^15,¹⁶ To transpose the vessel in the other variations of the far lateral approach, dissection and manipulation of the venous plexus around the VAs, which is sometimes referred to as the suboccipital cavernous sinus, is needed. The suboccipital cavernous plexus is connected to the suboccipital plexus through the suboccipital triangle and via the anterior vertebral vein.⁴ It is also connected to the internal vertebral venous plexus, posterior and anterior condylar veins, and occipital marginal sinus. To avoid intense bleeding from the plexuses, subperiosteal detachment of the VAs from its groove in C1 is recommended. To transpose the VAs, unroofing of the C1 transverse process is also mandatory. After detachment of the VAs and plexus, laminectomy of the C1 arch as laterally as possible can be performed to expose the OC for drilling.^1,^2,^4,^5,¹⁰

The V3 segment of the VAs has some branches that need to be coagulated during the approach. The first and largest is the anterior VAs, which passes through the suboccipital triangle to reach the muscles of the posterior neck. The posterior meningeal artery is another branch that can be coagulated. Care should be taken not to coagulate a posteroinferior cerebellar artery (PICA) or a posterior spinal artery that arises extradurally from the V3.

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