Introduction 63 3 13 15 19 55 64 9 13 15 19 24 25 56 60 61 7 The prerequisite for treating FM meningiomas (FMMs) is the perfect knowledge of the surgical anatomy. We will then first detail a comprehensive review of the relevant anatomy of the FM area with special emphasis on the vertebral artery (VA) V3 and V4 segments. Second, we will describe our classification system. This classification system helps for determining the best surgical approach and for anticipating the position of lower cranial nerves. The technical aspects of our surgical approaches will then be detailed extensively. Finally, we provide a summary of the relevant literature, detailing surgical results and surgical approaches advocated by other skull base surgeons and discussing the extent of bone resection and the need for fusion. Surgical anatomy Limits of the FM 13 18 19 1 Anterior border: lower third of the clivus and upper edge of the body of C2 Lateral borders: jugular tubercles and upper aspect of C2 laminas Posterior border: anterior edge of the squamous occipital bone and C2 spinous process Fig. 1 dotted line 1 2 3 4 5 6 7  The VA V3 and V4 segments The VA V3 and V4 segments are important vascular structures whose anatomy must be perfectly known when approaching FMMs. 8 8 8 50 11 33 43 50 50 50 8 8 8 12 29 36 23 26 30 40 53 12 36 48 23 47 The VA V4 segment ascends from the dura up to the anterior aspect of the pontomedullary sulcus where it joins the controlateral one to form the basilar artery. Initially, the VA V4 segment faces posteriorly and medially the occipital condyle, the hypoglossal canal, and the jugular tubercle. Later, the VA V4 segment lies on the clivus and runs in front of the hypoglossal and the lower cranial nerves rootlets. At the FM level, the VA V4 segment is at the origin of several branches: the PICA, the anterior spinal artery, the anterior and posterior meningeal arteries. 56 56 11 42 50 8 11 50 50 Lower cranial nerves 49 49 49 49 The dentate ligament The dentate ligament is a white fibrous sheet that extends from the pia mater, medially, to the dura mater, laterally. It forms arches leaving passage to the VA for the first one and the second cervical nerve root for the second one. Our classification system of foramen magnum meningiomas 2 Fig. 2 dotted lines  The definitive objective of a classification system is to define preoperatively the surgical strategy based on preoperative imaging characteristics of the lesion. The surgical strategy in cases of FMMs is the surgical approach but also the anticipation of modified vital structure position. 18 Intradural Extradural Intra- and extradural 31 32 39 56 60 62 Anterior, if insertion is on both sides of the anterior midline Lateral, if insertion is between the midline and the dentate ligament Posterior, if insertion is posterior to the dentate ligament Anterior meningiomas push the spinal cord posteriorly. Therefore, the surgical opening between the neuraxis and the FM lateral wall is narrow, and the drilling must extend to the medial part of the FM lateral wall to improve the access. In almost every case, no drilling of the lateral mass of the atlas and occipital condyle is necessary. Exceptionally, anterior meningiomas of small size without anterior compartment enlargement need more bone resection but never includes more than one fifth of these elements. On the other hand, lateral meningiomas displace the neuraxis posterolaterally and widely open the surgical access; therefore, the drilling has never to be extended into the lateral mass of the atlas or the occipital condyle. Above the VA Below the VA On both sides of the VA Meningiomas are more often located below the VA. In this case, the lower cranial nerves are always pushed cranially and posteriorly. There is no need to look for them. They will come into view on reaching the superior tumoral part. On the other hand, if the lesion grows above the VA, the position of the lower cranial nerves cannot be anticipated; the nerves may be displaced separately in any direction. After partial debulking of the tumor, one has to look for them so as to identify and protect them during the tumor resection. In case of tumoral development on both sides of the VA, a similar problem may exist with the position of the lower cranial nerves. Moreover, the dura around the VA penetration may be infiltrated by the tumor. As previously mentioned, the dura is normally adherent to the adventitia, and complete resection of the tumor at this level is hazardous. In this case, which is rarely observed, it may be safer to leave a cuff of infiltrated dura around the VA and to coagulate this zone. Surgical aspects Preoperative and perioperative considerations Standard preoperative workup includes magnetic resonance imaging (MRI), computed tomography (CT) scan, and sometimes angiography. On MRI, gadolinium-enhanced sequences help to precisely delimit the dural attachment zone, the tumor, and its relation to neural and vascular structures. On T2-weighted images, the presence of an arachnoid plane between the tumor and the neuraxis is sometimes visible. Bone windows CT scan is helpful in case of extradural extension to investigate bone erosion and to schedule preoperatively the need for fusion. If a highly vascularized tumor is suspected and embolization is contemplated To perform a balloon occlusion test in case of VA encasement (extradural or recurrent meningioma and meningioma inserted around the VA). In our experience, it has never been necessary to occlude the VA. 3 7 Surgical approaches and techniques at Lariboisière Hospital The midline posterior approach 15 17 The patient may be in the sitting, ventral, or lateral position. To decrease venous bleedings, the sitting position is preferred at Lariboisière Hospital as far as there is no contraindication such as a patent foramen ovale; air embolism is prevented by hypervolemia and G-suit. The skin is incised on the midline from the occipital protuberance down to the upper cervical region. The midline avascular plane is opened between the posterior muscles, up to the occipital protuberance and down to the spinous process of C2. Bone opening is performed using a drill and Kerrison rongeurs and is always limited to the lower part of the occipital bone and the posterior arch of the atlas. The dura is then incised in a T- or Y-shaped fashion and retracted with stitches. Postero-lateral approach 15 17 3 4 5 Fig. 3 a c d e f right side star arrow left side  Fig. 4 a b star c d  Fig. 5 a black arrow white arrowhead black arrowhead dotted line b black arrowhead white star black star c white arrow black arrowheads white arrowhead black star white star d left side white arrow black arrow black star black arrowhead  The postero-lateral approach is a lateral extension of the midline posterior approach. The patient must be carefully positioned in the same position as during a posterior midline approach. The head must be placed in neutral position. Any flexion must be avoided because it decreases the space in front of the neuraxis and therefore may worsen the compression and the neurological condition. The vertical midline skin incision is identical, but the incision is curved laterally on the tumoral side just below the occipital protuberance toward the mastoid process. The posterior muscles are divided along the occipital crest and retracted laterally to expose the occipital bone, the posterior arch of the atlas, and the C2 lamina, if required. The exposure may be extended on a limited way on the contralateral side. VA exposure 23 47 Bone opening The lateral extension of the bone opening is established according to the position of the meningioma. In case of lateral meningiomas, the spinal cord is displaced toward the contralateral side, and then any resection of the FM lateral wall is not necessary. In case of anterior meningiomas, the spinal cord is pushed posteriorly, and the surgical corridor has to be enlarged laterally by drilling up to the medial side of the C1 lateral mass and/or the occipital condyle. Drilling further the lateral mass of the atlas or the occipital condyle is exceptionally necessary. In the exceptional case where the opening must be enlarged, no more than 20% of the medial part of the FM lateral wall has to be drilled. In such a way, stabilization is never required. The cranio-caudal bone resection is scheduled according to the position of the tumor regarding to the VA. The drilling has to be extended toward the lateral mass of the atlas if the tumor grows below the VA, to the jugular tubercle and the occipital condyle if it grows above, and toward both parts of the FM lateral wall, if it encircles the VA on both sides. Dura opening Intradural step At this step, the surgical technique must be individualized according to the tumor location: above, below, or on both sides of the VA. As previously mentioned, in cases of tumor developed below the VA, the lower cranial nerves are always pushed cranially and posteriorly by the tumor. These nerves will then be found at the superior pole of the lesion at the end of the surgery. The resection must start at the caudal aspect of the meningioma with the goal to release the dural attachment and to suppress the vascular supply first; then, the tumor is debulked in a dry surgical field with a sucker, an ultrasound aspirator, or a laser, according to the tumor consistency. When liberating the dural insertion, it is important to keep undetached a small part of the base, at the side of the neuraxis, to avoid free movement of the lesion, which can be responsible for inadvertent damage to the neuraxis during the remnant resection. When hollowing the tumor, a small layer is also kept with its capsule against the neuraxis. This part will be resected at the last surgical step and under better conditions when the meningioma is completely devascularized and the surgical field widely open. If the tumor is developed above the VA, two special points must be taken into consideration: the displacement of the lower cranial nerves and the dissection of the VA branches. Indeed, in such location, the displacement of the lower cranial nerves cannot be anticipated. To prevent damage, the rootlets must be under control on the side of the jugular foramen and then followed along their courses more or less adherent to the meningioma. With the lesion being progressively debulked, the nerve rootlets can be more easily mobilized, often inferiorly, to allow a more confident tumor resection at some distance from fragile nervous structures. The tumor dissection from the VA branches, especially the PICA, is another difficulty encountered only with tumors developed above the VA. Precise knowledge of the patient anatomy based on preoperative investigation is mandatory. If the meningioma encases the VA, the technique is identical as described above. Special consideration is nevertheless required if the meningioma has its insertion on the dura surrounding the VA penetration. The dural resection is better achieved by progressing from the extradural side toward the intradural aspect, along the VA because the VA invaginates into the dura with its periosteal sheath. This furrow can be resected as much as the VA adventitia is not invaded. Dural closure Antero-lateral approach 15 17 8 Bone opening The exposure must now be adapted to each case, depending on the location and extension of the meningioma. The odontoid process can be reached by passing over the C1–C2 joint. The mastoid process can be resected and small bridging bone removed to open completely the jugular foramen from the end of the sigmoid sinus, to the jugular tubercle just underneath the junction with the jugular bulb, up to the beginning of the internal jugular vein. Dura opening Dural closure Postoperative complications The antero-lateral approach could induce a transient dysfunction of the accessory nerve by the nerve manipulation, responsible for pain along the trapezius muscle and weakness of the trapezius muscle and/or the SM muscle. During this approach, manipulation of the sympathetic chain could also be at the origin of a transient Horner’s syndrome. VA damage has never been observed. In case of tumoral encasement, a balloon occlusion test must be realized. Preservation of the lower CNs can be hazardous. If CN IX and X are damaged, postoperative swallowing problems must be anticipated. Review of the literature Published series 2 7 10 18 22 27 35 37 38 41 44 46 52 54 55 57 58 16 19 38 55 18 1 Table 1 Review of the literature of published series of FMMs over the last 20°years in the English literature Author Year Nb pt FMM location (%) Recurrence (%) Va encasement (%) Approach VA transp Resection JT Partial mast Nb CR (%) Extent CR Instability (%) Outcome (%) Resection (%) Transient morbidity (%) Permanent morbidity (%) Mortality (%) FU Recurr (%) Anterior Lateral Posterior Improved Unchanged Worsened Total Subtotal Gilsbach 1987 5  100    – FL  Y   1/3     100.0 0.0  20 0.0   Guidetti 1988 17 82.40                100.0   12 11.0   Sen, Sekhar 1990 5 80  20  80 – EL Y Y Y 100 1/3–1/2 0 20 20 60 60.0 40.0  60 20.0   Crockard 1991 3 100    33 33 TO No   0 0 33   100 0.0 66.0 100.0 100 66.0 20.6 33.0 Kratimenos 1993 8 100    12.50 – FL Y    1/3 0    87.5 12.5  0 25.0 – – Babu 1994 9  100     EL Y Y Y 100 1/3–1/2 0    88.8 11.2 78.0 56 11.1 9.4 0.0 Akalan 1994 8 12.50  87.50    PM    0 0  88 12  100.0   0 0.0   Bertalanffy 1996 19  100    – FL SO TC  Y  100 1/3 0    100.0 0.0  0 0.0 – – Samii 1996 38  95  5 5 40 PM, LSO    17.50 1/3 0    63.0 30.0 37.0 5 6.0 21.0 5.0 George 1997 40 45  52.50 2.50  38     100 Partial 0 90 2.50 7.50 87.5 10.0  0.00 7.5 57.6 0.0 Pirotte 1998 6  100    –  Y   100 1/2–1/3 0    100.0 0.0  17 17.0   Sharma 1999 10 50   50   PM, FL    0 0 Yes    100.0    15.0   Salas 1999 24  100    – TC/ELTJ Y  Y 100 1/3 0    66.0 33.0  – 0.0 14.8 – Arnautovic 2000 18 100    11.10 – TC Y   100 1/2–1/3 0 89 11  75.0 12.5 55 11.1 16.6 40.0 5.5 Roberti 2001 21       EL TC          76.0 24.0  21.50 9.5   Goel 2001 17  100    59 SO    11.80 1/3–1/4 0 100   82.0 18.0  6 0.0   Nanda 2002 6 100     – FL    0 0  100   100.0 0.0  0 0.0 43.0 0.0 Marin Sanabria 2002 7  72.50  28.50   TO, SO, TC    29 1/3–1/2 0 80.00  20 100.0 0.0 72.5 5 14.0   Parlato 2003 7      –  Y    <1/2 0    86.0% 14.0   0.0 24.0 0.0 Boulton 2003 10 60  10 30       0 0  70 20 10 90.0 10.0 40.0 10 0.0   Pamir 2004 22  91  9  40 FL    95 1/3 0    95.5 4.5 27 4.50 0.0 40.0 0.0 Margalit 2005 18  100     Lat    50 Partial (9/18)         0.0   Bassiouni 2006 25 32  57 11 4 43 FL    0 0     96.0 4.0 40.0 8 4.0 73.2 0.0 CR EL FMM FL FU JT mast Lat Nb pt Recurr SO TC TO transp VA Y Heterogenicity of published series 2 4 10 35 38 41 45 57 58 1 2 3 27 41 4 6 20 21 35 44 46 54 55 57 5 7 18 37 44 55 58 21 57 1 Surgical approaches, extent of bone resection, and need for fusion FMMs are undoubtedly challenging tumors, requiring special considerations because of the vicinity of the brainstem, medulla oblongata, lower cranial nerves, and the VA. Several approaches have been advocated. The definite goals are to achieve the largest tumor removal and the lowest morbidity rate as possible. Minimizing the morbidity is obtained by choosing the appropriate exposure. The approach must allow adequate controls of important neurovascular structures, without exposing to unnecessary risks. There is no discussion about the best surgical approach of posterior FMMs. The posterior approach is the best option, is well known by neurosurgeons, and is associated with a low morbidity rate. The debate about the best surgical approach is more open for lateral and mainly anterior FMMs. 10 39 10 39 28 51 57 4 52 54 54 4 54 57 3 3 4 27 45 54 57 5 6 20 21 27 35 41 44 55 58 46 27 41 44 46 55 5 1 2 5 7 21 35 37 41 55 58 21 35 37 55 2 5 7 41 58 2 41 58 5 7 2 5 7 41 2 15 Surgical results Morbidity–mortality–prognosis factors 34 1 4 27 37 46 57 58 1 3 5 55 18 55 18 22 5 14 65 4 5 55 57 Rate of tumoral resection 19 2 4 7 10 18 22 27 35 37 41 44 46 52 54 57 58 3 55 57 5 18 3 3 5 18 21 44 55 55 19 39 19 Our experience 18 41 1 59 Conclusions FMMs are challenging tumors in the vicinity of the brainstem, the VA, and lower cranial nerves. Several surgical approaches are possible, each one with specific indications. The drilling of the FM lateral wall required during the approaches is always limited and by itself should not be at the origin of any instability. Postoperative complications can be dramatic and must be anticipated.