International Journal of Neurooncology

REVIEW ARTICLE
Year
: 2021  |  Volume : 4  |  Issue : 3  |  Page : 65--75

Surgical management of benign tumors at the foramen magnum region


Laligam N Sekhar, Varadaraya S Shenoy, Zeeshan Qazi 
 Department of Neurological Surgery, University of Washington, Seattle, Washington, USA

Correspondence Address:
Dr. Laligam N Sekhar
Department of Neurological Surgery, University of Washington, 325 Ninth Ave, Box 359924, Seattle, Washington 98104
USA

Abstract

Tumors in the foramen magnum region are among the most challenging neurosurgical lesions to operate. They may be divided into intradural and extradural tumors, which have differing pathologies. Meningiomas represent the most common intradural tumor in this region. Anatomical constraints caused by adjacent critical areas of the brainstem, proximity to the lower cranial nerves (CNs), and vertebral arteries add to the complexity and make total tumor resection difficult without damaging the brain stem, CNs, or the vertebral artery and branches. This review article summarizes the surgical approaches and relevant anatomical landmarks with illustrations at each step. We also illustrate with example cases, the decision-making process and highlight key strategies for the safe resection of these tumors.



How to cite this article:
Sekhar LN, Shenoy VS, Qazi Z. Surgical management of benign tumors at the foramen magnum region.Int J Neurooncol 2021;4:65-75


How to cite this URL:
Sekhar LN, Shenoy VS, Qazi Z. Surgical management of benign tumors at the foramen magnum region. Int J Neurooncol [serial online] 2021 [cited 2022 Jan 27 ];4:65-75
Available from: https://www.Internationaljneurooncology.com/text.asp?2021/4/3/65/329806


Full Text



 Introduction



The foramen magnum region extends from the jugular foramen superiorly down to the C1 level inferiorly. Important anatomical structures include the medulla and the spinal cord, cranial nerves (CNs) X, XI, and XII, spinal nerves C1 and C2, vertebral arteries and their anterior spinal and the medullary branches, the spinal medullary veins, and their drainage channels, the dural sheath that encloses the terminus of the brainstem and the spinal cord, the bony canal of the foramen magnum and the C1 vertebral arch.[1] It should be noted that the shape of the foramen magnum is variable from oval to circular shape, and this sometimes determines the surgical approach as well.[1]

Benign tumors at the foramen magnum region could be extra- or intra-axial. An extra-axial lesion could be lateral, anterolateral, or anterior to the spinal-medullary junction, and very rarely, posterior. Intra-axial tumors may be central or centrolateral inside the spinal cord and the medulla

The following are the key considerations with regard to surgery:[2],[3],[4],[5]

The superior and inferior extension of the tumorThe lateral extension of the tumorRelationship to the vertebral artery (VA) (V3 and V4 segment), whether or not the main VA and its perforators are encased by the tumorPrior surgery or radiotherapyPatient's functional status with respect to swallowing, independence, and working ability.

Extra-axial lesions are most commonly meningiomas, which can be located laterally, anterolaterally, or purely anteriorly.[6],[7],[8] Other tumors presenting as extra-axial mass include schwannomas of the hypoglossal nerve and C1 root schwannomas, hemangioblastomas, and cysts including neurenteric cyst or synovial cysts.[7] Intra-axial tumors include hemangioblastomas, ependymomas, subependymomas, and some types of cysts.

The clinical presentations of all benign tumors at the foramen magnum region are similar.[7],[8] They include headache, gait deterioration, swallowing, and speech difficulties. Severe failure of swallowing and speech, hemiparesis, or quadriparesis appear late in the course.[6],[7],[8] Neurological examination may reveal deficits in CNs X, XI, and XII, ataxia, paresis of arms or legs, dysarthria, and swallowing problems.[6],[8] Even if the patients do not present with these symptoms, one should examine the patient carefully for neurological deficits since they may become more marked after the surgery.

 Investigation



During the workup of patients, it is important to find out the patient's goals with regard to the resection. This includes whether they prefer to have partial removal with functional preservation or an attempted total resection even if it means some transient or permanent CN deficits. Magnetic resonance imaging (MRI) is important, and one should evaluate the arachnoid plane and also look for hydrocephalus and contrast enhancement. Computed tomography (CT) scan with bone window shows is important. CT angiography and CT venography can be performed to evaluate bilateral vertebral arteries, venous sinuses, and jugular bulbs. Intra-arterial digital angiography with possible embolization is often performed for larger, more vascular tumors. If embolization is performed, it should be safe and must not risk damage to major vessels or perforator vessels. Feeding blood vessels may be derived from the ascending pharyngeal artery, posterior meningeal or other branches of the VA, and rarely meningohypophyseal artery. If the vessel can be embolized without risking the brainstem or the lower CNs, it must be done.

 Treatment Approaches



Microsurgical resection is the main treatment modality for benign tumors in the foramen magnum region.[3] Endoscope is used for visualization (and sometimes resection) assistance to microsurgery. A ventriculoperitoneal (VP) shunt may be needed in the postoperative period if hydrocephalus persists. Radiosurgery can be employed for small tumor remnants.

There are various approaches for microsurgical resection. The use of a particular approach depends on the location of the tumor in the foramen magnum region, whether the tumor is in the midline, lateral, posterior, or anterior, and also whether or not it is intra- or extra-axial.[3],[9]

For posteriorly and centrally placed midline lesions, we use midline suboccipital craniotomy with C1-C2 laminectomyA far lateral approach is commonly used for laterally placed benign tumors in this area. It exposes the V3 segment of the VA up to or including the sigmoid sinus. It is retrocondylar, i.e. there is no drilling of the occipital condyle or the C1 lateral mass, and the VA is exposed but not displaced from its locationAn extreme lateral partial transcondylar approach is used for tumors that are both anterior and anterolateral. The surgeon performs partial resection of the occipital condyle (generally up to half of the occipital condyle) and the C1 lateral mass. Jugular tubercle may be resected as needed. The terminal V2 and V3 segments of the VA are exposed and may be displaced medially to facilitate the exposure and to protect the arteryA complete transcondylar approach that includes complete removal of the occipital condyle and the lateral mass of C1 is rarely used only for the very anteriorly located small extra-axial tumors in the foramen magnum region, without any lateral access, especially when both hypoglossal nerves are involved by the tumorA transoral approach, either open approach or endoscopic, is not used for benign tumors because of some problems. It provides inadequate exposure for complete resection; any vascular injury is difficult to manage, postoperative cerebrospinal fluid (CSF) leak is difficult to seal and may result in meningitis.

 Anesthesia and Monitoring



We use intravenous anesthesia, monitoring of multiple CNs as needed, as well as neuromonitoring with somatosensory-evoked potentials and motor-evoked potentials.

 Position



For far lateral or extreme lateral approaches, the patient is typically in the full lateral position with the arm off the table, well supported and padded, and the head is held in the neutral position [Figure 1], [Figure 2], [Figure 3]. One can turn the head toward the floor or the surgeon slightly, but for most of the patients, we keep the head in the neutral position.{Figure 1}{Figure 2}{Figure 3}

The extreme lateral and far lateral approaches are described below in some detail.

 Surgical Exposure: Skin Incision and Muscle Dissection



Two types of incisions can be used for tumors in the foramen magnum region. One is an inverted U-shaped incision, starting laterally and extending to the midline where the muscle layers are reflected along with the skin flap. However, if one wants to be very lateral, the senior author prefers to make a C-shaped incision [Figure 2]a, and the skin flap is reflected along with the sternocleidomastoid (SCM) muscle and fascia so that the vascularity is well preserved. This exposes different layers of the muscle deep to it. The first later is the SCM muscle [Figure 2]b reflected with the skin flap. The second layer is the splenius capitis muscle [Figure 2]c, reflected medially and inferiorly. The layers of muscles can be distinguished by the direction of their fibers. We like to detach the muscles from their attachment and reflect them inferiorly. The third layer consists of the longissimus capitis and semispinalis capitis muscles [Figure 2]c. Between the second and the third layer runs horizontally, the occipital artery (OA) which can be dissected and preserved; it can be used in cases where an OA to posterior inferior cerebellar artery (PICA) bypass is necessary. Then, we reach the fourth layer, which consists of muscles in the sub-occipital triangle [Figure 2]d. These include superior and inferior oblique and rectus capitis major muscles, which form the suboccipital triangle. When we are at the fourth layer, we will visualize the VA and the venous plexus.

 Landmarks for the Vertebral Artery



The V3 segment of the VA superior to the C1 arch can be identified by several landmarks [Table 1]. The C1 lamina is a landmark. There is a venous plexus around it [Figure 2]d. One can use Doppler as well. The terminal V2 segment of the VA between the C1 and C2 foramina can be identified easily in some patients as it is crossed posteriorly by the C2 root, which is also useful. It is very important to find the VA and carefully preserve it.{Table 1}

 Vertebral Artery Translocation



Once the VA is identified, if one wants to displace it, the C1 foramen must be unroofed, with preservation of the periosteum and the venous plexus. The VA is dissected all the way from the C2 foramen or from the C2 root crossing point and displaced medially. A diamond drill, an ultrasonic bone dissector, and fine rongeurs are used in the process. It may be necessary to control the venous bleeding by bipolar cautery or by injection of small amounts of fibrin glue into the venous plexus. The medial displacement of the VA is very helpful for tumors which are located quite anterior and anterolateral to the cord, or if the VA is encased by the tumor. The surgeon can trace the VA through its dural entrance point intradurally and dissect it free. Sometimes, the PICA can be originating in this region, extradurally, or just after dural entry of the VA. In such cases, the PICA is carefully preserved. The anatomical dissection in [Figure 2] shows the VA translocated with the dural incision having been made around it. The artery can be flipped on either side, and the surgeon can have good exposure anterior to the spinal cord, all the way to the contralateral VA and visualize the anterior spinal artery.

 Tumor Resection



In most patients, the tumor resection is started in the space between the C1 root and the hypoglossal or the vagus nerve (lowest fibers). The VA and its branches should be identified and dissected free. The tumor is debulked and disconnected completely from the dural attachment. The next step is the dissection from the spinal cord and the medulla, respecting the arachnoid plane. In some patients, tumor pieces may need to be left around the lower CNs as they exit the jugular foramen to preserve their function.

 Reconstruction



Reconstruction is important to prevent a postoperative CSF leak. We generally use a dural substitute or temporalis fascia to repair the dural defect. The dural graft may be cut accordingly and loosely sutured to the adventitia around the VA as it enters the dura. This is supplemented by the fibrin glue. The muscle layers are replaced as physiologically as possible, and if there is a bone defect in the suboccipital area, titanium mesh can be used for cranioplasty.

Limiting factors for resection of benign tumors in the foramen magnum region include the following:[8]

Pial invasion of the medulla or the spinal cordEncasement of the perforating vessels or the anterior spinal arterySevere adhesion of the tumor to the anterior spinal veinRecurrence of the tumor with scar formationSurgeon's desire to preserve the function in CNs X, XI, and XII. A small piece of tumor may be left behind.

Potential complications and management

Medullary and spinal cord injuries are very rareVA injury can occur and requires immediate reconstruction by resuture or a short graftSmall artery branch injuries can occur, which may be managed with temporary clips and suture if possibleInjury can occur to the CNs, particularly X, XI, and XII. If there is bilateral CN XII palsy, it will create a very severe situation with dysphagia, and the patient may require a gastrostomy. Tracheostomy is very rarely needed even if there is X or XI weaknessCSF effusion with pseudo-meningocele formation or CSF leakage from the wound may occur rarely; the patient may require a shunt procedure such as the VP shunt. Sometimes, one has to shunt directly from the effusion site in a “T” fashionInfections may occur which requires bone removal and antibiotics.

 Summary



A summary of benign tumors at the foramen magnum region operated by the senior surgeon (LNS) from March 2005 to December 2020 is listed in [Table 2]. Over a period of 25 years, more than 100 meningiomas were operated at the foramen magnum region. There were two deaths; One due to severe vasospasm, and another due to aspiration pneumonia from lower CN paralysis. In the majority of cases, complete or near-complete resection was achieved [Table 3].{Table 2}{Table 3}

 Illustrative Cases



Case 1: Large cervicomedullary hemangioblastoma

A 37-year-old male presented with progressive right-sided hemiparesis for 6 months. Neurological examination revealed grade 4/5 motor power on the right side and bilateral hyperreflexia. MRI revealed a very large eccentric cervicomedullary hemangioblastoma, extending from the medulla laterally down along the right cervical cord to about the lower border of C2 [Figure 4] and [Figure 5]. Preoperative cerebral angiogram revealed multiple feeders, mainly the anterior spinal artery and lateral spinal artery branch vessels, supplying the tumor mass [Figure 6]. CT imaging showed the location of the tumor and its relation to the VA quite nicely [Figure 7]. Preoperative polyvinyl alcohol (PVA) embolization of feeders from the lateral spinal artery was performed to partially devascularize the tumor but was not very helpful during the surgery. The surgery involved a far lateral approach and a C1-C3 laminectomy with the patient in a right side up lateral decubitus position. A right-sided retro-sigmoid craniotomy and craniectomy was performed. The right VA V3 segment was exposed, but we did not have to displace the VA. C1 and C2 hemilaminectomy was done, and we were able to expose the tumor. The tumor resection proceeded as can be seen in [Figure 8] and [Figure 9]. Following durotomy, we saw the tumor and the C1-C2 rootlets. The tumor was quite vascular with arteries entering it at multiple places. A very prominent artery arising from the VA supplying the tumor in the medullary region was temporarily occluded with a clip [Figure 9]a. We developed a dissection plane around the tumor [Figure 9]b and [Figure 9]c; The tumor was surrounded by gliotic tissue and a cyst. We entered the cyst, and the tumor was devascularized, circumferentially dissected, and removed totally [Figure 9]d. The patient did well postoperatively. He developed hyponatremia and postural hypotension. He made a nearly complete recovery with mild right-sided weakness and he has not had any recurrence for more than 4 years [Figure 10]a, [Figure 10]b, [Figure 10]c.{Figure 4}{Figure 5}{Figure 6}{Figure 7}{Figure 8}{Figure 9}{Figure 10}

Case 2

Large and complex lower clival foramen magnum and C1 location meningioma, with significant brain stem compression, and extension toward both hypoglossal nerve canals.

A 54-year-old female presented with some neck pain as well as bilateral hand tingling and numbness, and during the investigation, she was found to have an extensive, predominantly anterior, foramen magnum meningioma. Preoperatively, she had paraparesis, as well as numbness above the level of the nipple line in the chest and both arms, left worse than right. The tumor caused very significant brain stem compression [Figure 11]a, [Figure 11]b, [Figure 11]c.{Figure 11}

The challenges in this case were as follows

Exposure of the lesion without retracting the brain stemAt least one VA was going through the tumor [Figure 12]a, [Figure 12]b, [Figure 12]c, [Figure 12]dPreservation of bilateral hypoglossal nerve function.{Figure 12}

In a patient like this, when embolization can be safely performed, it is helpful. Normally, these tumors are supplied by ascending radicular branches of the VA or the ascending pharyngeal artery [Figure 12]e. Ascending pharyngeal artery embolization is tricky because of the shared blood supply with the lower CNs. If embolization is done, one should use larger PVA particles (350–500 microns) to avoid damage to the neuromeningeal trunk.

The patient was operated through a left-sided extreme lateral approach with partial removal of the condyle and C1 lateral mass. The VA was displaced medially [Figure 13]a, [Figure 13]b, [Figure 13]c, [Figure 13]d, [Figure 13]e, [Figure 13]f. We began to debulk the tumor in the foramen magnum C1 region. The tumor was calcified. Initial debulking was accomplished with the CO2 laser, but subsequently, we used the Sonopet® ultrasonic bone curette [Figure 13]d. The tumor was gradually removed between the rootlets of CNs X, XI, and XII. We were able to achieve near-total resection, gradually removing the tumor in the midline and then going across. There was a very large portion of the tumor base that was ossified. This was removed with the Sonopet® ultrasonic bone curette, as well as with the soft-tissue Sonopet®, and then cauterized. The removal of this part was quite difficult. Contralateral VA, C1 rootlets, and the hypoglossal rootlets were identified and carefully preserved. We had to leave a small residue right at the exit point of the lower CNs to preserve that function [Figure 14]a, [Figure 14]b, [Figure 14]c. She did well without any postoperative problems.{Figure 13}{Figure 14}

Case 3: Large foramen magnum meningioma with dominant occipital sinus

This patient is a 62-year-old male, who had a tumor that was not only central but also extended well up into the midclival area [Figure 15]a, [Figure 15]b, [Figure 15]c. The patient underwent angiography preoperatively. The tumor received blood supply from the ascending pharyngeal artery as well as from the branch of the OA. In addition, what was importantly seen on the angiogram, is that patient had a very prominent occipital sinus that connects with the circular sinus. The transverse sinus and the sigmoid sinus are very small bilaterally [Figure 16]a. This illustrates the importance of angiography for patients with larger tumors. In this patient, if one were to damage the circular sinus, then the patient could have had a major venous infarction [Figure 16]a, [Figure 16]b, [Figure 16]c, [Figure 16]d.{Figure 15}{Figure 16}

The patient underwent preoperative embolization through the ascending pharyngeal artery. The surgery was performed in two stages. The first one was a right-sided extreme lateral partial trans-condylar approach. The main problem here was that we could not open the retro-sigmoid dura completely because of the very large and prominent circular sinus [Figures 16]a. The entire operation was done through a window between the venous sinus and the C1 nerve root [Figure 17]. About 2/3rd of the tumor was excised.{Figure 17}

Postoperative MRI showed a significant tumor residue in the midclival region [Figure 18]a, [Figure 18]b, [Figure 18]c, [Figure 18]d. Therefore, we decided to operate by a retro-sigmoid and presigmoid approach with complete unroofing of the very small transverse sinus. Hence, we could reflect that sinus laterally by the extensive bone drilling; and then we had a very lateral approach, as can be seen in [Figure 19]a and [Figure 19]b. Although we did a complete posterior petrosal approach with a temporal craniotomy, it was not necessary; we used both the retrosigmoid and presigmoid approaches to the tumor, and we were able to access it very nicely. During this operation, we also used a neuro-endoscope for endoscopic assistance and evaluation to make sure we had complete or near-complete resection. The patient had a gross total tumor resection [Figure 20]a and [Figure 20]b. Postoperatively, he developed bilateral tongue weakness which improved. He also needed a vocal cord injection and a gastrostomy. All symptoms resolved after 3 months.{Figure 18}{Figure 19}{Figure 20}

Case 4: Recurrent meningioma with occluded vertebral artery

A 65-year-old female presented with recurrent meningioma and previously occluded VA by another surgeon [Figure 21]a and [Figure 21]b. She presented in a very poor condition with a tracheostomy and quadriparesis and was transferred to us for further treatment. She underwent complete resection. One VA was completely occluded from previous surgery. However, on postoperative day 13, she suffered a severe neurological decline [Figure 22]a, [Figure 22]b, [Figure 22]c. CT scan showed bilateral cerebellar infarcts [Figure 22]c. We performed an angiogram and that showed she had suffered a significant spasm of the VA [Figure 22]a and [Figure 22]b. She underwent angioplasty, but it was too late in her course, and she eventually died. This case highlights the point that patients can have vasospasm, especially in recurrent cases, and so we have to be watchful of these patients.{Figure 21}{Figure 22}

Case 5: Occipital-cervical instability after surgery for foramen magnum meningioma

The case illustrates a rare complication. A 63-year-old female was followed up for an asymptomatic meningioma. The tumor had grown over 7 years and caused a significant compression in the spinomedullary junction. However, the patient did not have any neurological deficits. The patient decided to undergo surgery on our recommendation. The tumor was located quite anteriorly slightly eccentric to the left side. We operated her with a left-sided extreme lateral approach. The approach was from the left side rather than the right because the brainstem was slightly distorted to the left side [Figure 23]a, [Figure 23]b. During the surgery, we ended up removing more occipital condyle to get anterior. More than two-third of the condyle was removed along with the C1 lateral mass [Figure 24]a, [Figure 24]b, [Figure 24]c, [Figure 24]d, [Figure 24]e. Postoperatively, the patient developed a neck tilt and some neck pain due to excessive resection of the left occipital condyle and C1 lateral mass [Figure 24]e. Therefore, we had performed an occipital to C1 fusion 1 month after the original surgery, which completely resolved her symptoms. At a 2-year follow-up, she was asymptomatic [Figure 25]a, [Figure 25]b, [Figure 25]c, [Figure 25]d, [Figure 25]e, [Figure 25]f, [Figure 25]g.{Figure 23}{Figure 24}{Figure 25}

Case 6: Large hypoglossal schwannoma

A 37-year-old male presented with a history of left-sided tongue atrophy and fasciculations and weakness of upper limbs for 3 months. MRI revealed a large, partially cystic tumor with severe compression of the brainstem and spinal cord, with expansion and erosion of the hypoglossal canal [Figure 26]a, [Figure 26]b, [Figure 26]c. CT angiography showed the left VA to be anteriorly displaced by the tumor [Figure 26]d and [Figure 26]e. CT scan bone window showed the dilated hypoglossal canal [Figure 26]f.{Figure 26}

His hypoglossal nerve function was intact on the left side. Our goal was to preserve the hypoglossal nerve function in addition to the removal of the tumor. He was operated on by an extreme lateral and partial transcondylar approach. A small tumor remnant was left inside the hypoglossal canal to preserve the nerve, and subsequently, this was treated by radiosurgery [Figure 27]. His modified Rankin Score was 1 at 6-month follow-up, and tongue function was preserved.{Figure 27}

 Conclusions



In this article, we have described various types of intradural tumors at the foramen magnum which are predominantly benign, and the lateral approaches. The midline suboccipital craniotomy, C1 laminectomy approach is not described since it is well known to neurosurgeons.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

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