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The V3 segment of the vertebral artery: Surgery around the craniocervical junction

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The V3 Segment of the Vertebral Artery: Surgery Around the Craniocervical Junction Bernard George, MD, Alexandre Blanquet, MD, and Oscar Alves, MD Exposure of the third segment (V3) of the vertebral artery (VA) is more challenging than at lower levels because of its complex course around the craniocervical junction. Surgical control of the VA may be usefut in treating lesions in close relation with the VA and inducing a more or less important compression. Like com- pression at lower levels, compression at V3 may be intermittent or permanent. Intermittent compression is usually related to bony or ligamentous anomalies or to a rotational mechanical obstruc- tion (bow hunter's syndrome). Permanent compression is typi- cally caused by neuromeningeal or bone tumors. Surgical expo- sure of the VA with or without transposition allows different areas to be accessed. The intradural foramen magnum can be reached via the posterolateral approach, and the jugular foramen and the anterior part of the craniocervical junction (CCJ) can be reached via the juxtacondylar approach. At the CCJ the elements that help stabilize the CCJ must be respected when they are intact. Preoperative planning requires choosing the surgical route that provides access to the lesion without compromising stability. Copyright 2002, Elsevier Science (USA). All rights reserved. T he third segment (V3) of the vertebral artery (VA) has a complex course around the craniocervical junction (CCJ). As at the level of V2, control of the VA may be useful for treating nearby compressive lesions. Control of the VA also helps gain better access to different regions: the anterior part of the CCJ, foramen magnum, and jugular foramen. External Compression of the VA Lesions close to V3 can cause either intermittent or permanent compression. Intermittent Compression Typically, intermittent compression at V3 is related to nontu- moral lesions like those that involve V2.1 Spondylosis, how- ever, is much less common at C1 or C2 than lower in the neck. Factors that cause transitory compression at V3 are most of- ten congenital bony and tendinous malformations (Fig 1, Table 1).~.3,* A particular movement of the head and the neck always produces the symptoms. During angiography this movement From the Department of Neurosurgery, H6pital Lariboisiere, Paris, France. Address reprints requests to Bernard George, Department of Neuro- surgery, H6pital Lariboisiere, 2 rue Ambroise Pare, 75010 Paris, France, Tel: 33 1-49-95-81-46 Fax: 33 1-49-95-81-55 E-mail: bernard.george@ Irb.ap-hop-paris.fr Copyright 2002, ElsevierScience (USA). All rights reserved. 1092-440X/02/0501-0001535.00/0 doi:10.1053/otns.2002.0000 must be repeated and must induce severe stenosis of the VA. These two conditions, the same movement producing symp- toms and inducing angiographic compression, must be verified before pursuing surgical decompression of the VA. The move- ment that induces the compression is often complex, combin- ing flexion and rotation toward the opposite side. Angiographic study of cadavers 5,6,7 and living patients 8.H have shown that a combination of extension and rotation of the head in the phys- iological range of motion can occlude the VA. This condition is sometimes called rotational mechanical obstruction. When it is symptomatic, it is called bow hunter's syndrome. 3,12-~4 In fact, cases involving subluxation of the C1-C2 joint and cases in- volving compression by fibrous bands, ~5 a thickened atlanto- occipital membrane, 5 or bony anomalies a6,1z have been pub- lished under this name. However, the term bow hunter's syndrome should be reserved for cases of VA obstruction caused by excessive sliding of the atlas in relation to the axis. These two groups of patients can be differentiated with the 3D CT angiography, which shows the relation between bone and vessels when the head is in different positions. Other causes of intermittent occlusion of V3 are subluxation of the C1-C2 joint regardless of its originlS-ZZ: a malformation as in os odontoideum, degeneration, inflammation as in rheu- matoid arthritis, or traumatic injury. Besides malformations inducing spinal instability, some bony malformations may in- termittently compress the VA. We have observed two cases of bony malformation of the C1-C2 joint compressing the VA in the C2 transverse foramen, three cases of abnormal piece of bone suggesting a supplementary condyle at the level of the C0-C1 joint (occipital condyle-lateral mass of atlas) and a case of Klippel-Feil with fusion of the posterior arch of atlas with the C2 laminae. Intermittent compression at V3 often produces more dramatic symptoms than at V2. At V3, it is unlikely that the muscular arterial network can compensate for the de- creased blood flow in the VA. Of our 6 cases, 3 completely lost consciousness and exhibited brain stem signs. One patient had multiple small cerebellar infarcts visible on MRI (Fig 2). One of our patients had tuberculosis involving the atlas and compressing both VAs with complete occlusion on one side and severe stenosis on the other side (Fig 3). 1 The patient was referred after five transient ischemic attacks of the vertebrobasi- lar system. After medical treatment and immobilization of the neck with a halo-vest, all symptoms resolved and both VAs regained their normal aspect. The second cervical nerve root crossing the C1-C2 portion of the VA also can compress the VA during controlateral rotation of the head. One case has been reported in the literature, a,23 and we have observed a similar case. It is difficult to understand why the C2 root becomes compressive in some patients. In our patient, the compression was clearly demonstrated during sur- gery by release of the VA after the C2 root was sectioned. 50 Operative Techniques in Neurosurgery, Vol 5, No 1 (March), 2002: pp 50-74
Transcript
Page 1: The V3 segment of the vertebral artery: Surgery around the craniocervical junction

The V3 Segment of the Vertebral Artery: Surgery Around the Craniocervical Junction

Bernard George, MD, Alexandre Blanquet, MD, and Oscar Alves, MD

Exposure of the third segment (V3) of the vertebral artery (VA) is more challenging than at lower levels because of its complex course around the craniocervical junction. Surgical control of the VA may be usefut in treating lesions in close relation with the VA and inducing a more or less important compression. Like com- pression at lower levels, compression at V3 may be intermittent or permanent. Intermittent compression is usually related to bony or ligamentous anomalies or to a rotational mechanical obstruc- tion (bow hunter's syndrome). Permanent compression is typi- cally caused by neuromeningeal or bone tumors. Surgical expo- sure of the VA with or without transposition allows different areas to be accessed. The intradural foramen magnum can be reached via the posterolateral approach, and the jugular foramen and the anterior part of the craniocervical junction (CCJ) can be reached via the juxtacondylar approach. At the CCJ the elements that help stabilize the CCJ must be respected when they are intact. Preoperative planning requires choosing the surgical route that provides access to the lesion without compromising stability. Copyright 2002, Elsevier Science (USA). All rights reserved.

T he third segment (V3) of the vertebral artery (VA) has a complex course around the craniocervical junction (CCJ).

As at the level of V2, control of the VA may be useful for treating nearby compressive lesions. Control of the VA also helps gain better access to different regions: the anterior part of the CCJ, foramen magnum, and jugular foramen.

External Compression of the VA

Lesions close to V3 can cause either intermittent or permanent compression.

Intermittent Compression

Typically, intermittent compression at V3 is related to nontu- moral lesions like those that involve V2.1 Spondylosis, how- ever, is much less common at C1 or C2 than lower in the neck. Factors that cause transitory compression at V3 are most of- ten congenital bony and tendinous malformations (Fig 1, Table 1).~.3,*

A particular movement of the head and the neck always produces the symptoms. During angiography this movement

From the Department of Neurosurgery, H6pital Lariboisiere, Paris, France.

Address reprints requests to Bernard George, Department of Neuro- surgery, H6pital Lariboisiere, 2 rue Ambroise Pare, 75010 Paris, France, Tel: 33 1-49-95-81-46 Fax: 33 1-49-95-81-55 E-mail: bernard.george@ Irb.ap-hop-paris.fr

Copyright 2002, Elsevier Science (USA). All rights reserved. 1092-440X/02/0501-0001535.00/0 doi:10.1053/otns.2002.0000

must be repeated and must induce severe stenosis of the VA. These two conditions, the same movement producing symp- toms and inducing angiographic compression, must be verified before pursuing surgical decompression of the VA. The move- ment that induces the compression is often complex, combin- ing flexion and rotation toward the opposite side. Angiographic study of cadavers 5,6,7 and living patients 8.H have shown that a combination of extension and rotation of the head in the phys- iological range of motion can occlude the VA. This condition is sometimes called rotational mechanical obstruction. When it is symptomatic, it is called bow hunter's syndrome. 3,12-~4 In fact, cases involving subluxation of the C1-C2 joint and cases in- volving compression by fibrous bands, ~5 a thickened atlanto- occipital membrane, 5 or bony anomalies a6,1z have been pub- lished under this name. However, the term bow hunter's syndrome should be reserved for cases of VA obstruction caused by excessive sliding of the atlas in relation to the axis. These two groups of patients can be differentiated with the 3D CT angiography, which shows the relation between bone and vessels when the head is in different positions.

Other causes of intermittent occlusion of V3 are subluxation of the C1-C2 joint regardless of its originlS-ZZ: a malformation as in os odontoideum, degeneration, inflammation as in rheu- matoid arthritis, or traumatic injury. Besides malformations inducing spinal instability, some bony malformations may in- termittently compress the VA. We have observed two cases of bony malformation of the C1-C2 joint compressing the VA in the C2 transverse foramen, three cases of abnormal piece of bone suggesting a supplementary condyle at the level of the C0-C1 joint (occipital condyle-lateral mass of atlas) and a case of Klippel-Feil with fusion of the posterior arch of atlas with the C2 laminae. Intermittent compression at V3 often produces more dramatic symptoms than at V2. At V3, it is unlikely that the muscular arterial network can compensate for the de- creased blood flow in the VA. Of our 6 cases, 3 completely lost consciousness and exhibited brain stem signs. One patient had multiple small cerebellar infarcts visible on MRI (Fig 2).

One of our patients had tuberculosis involving the atlas and compressing both VAs with complete occlusion on one side and severe stenosis on the other side (Fig 3). 1 The patient was referred after five transient ischemic attacks of the vertebrobasi- lar system. After medical treatment and immobilization of the neck with a halo-vest, all symptoms resolved and both VAs regained their normal aspect.

The second cervical nerve root crossing the C1-C2 portion of the VA also can compress the VA during controlateral rotation of the head. One case has been reported in the literature, a,23 and we have observed a similar case. It is difficult to understand why the C2 root becomes compressive in some patients. In our patient, the compression was clearly demonstrated during sur- gery by release of the VA after the C2 root was sectioned.

5 0 Operative Techniques in Neurosurgery, Vol 5, No 1 (March), 2002: pp 50-74

Page 2: The V3 segment of the vertebral artery: Surgery around the craniocervical junction

Fig 1. Intermittent compression of the V3 segment during rotation and lateral tilting of the head, A bony malformation of the condyle seen on an axial CT scan (A) can be seen compressing the VA in the groove of the atlas on angiogra- phy (B).

Permanent Compression

Permanent compression is related to tumors of various origins (Table 2). Neuromenirlgeal tumors are mostly represented by neurinomas (Fig 4). At C1-C2, neurinomas have an extradural component much more frequently than at any other level of the spine. 24,25 In fact, about 85% of C1 and C2 neurinomas are either completely extradural or intra- and extradural while only 15% are strictly intradural. Neurinomas of the C 1 nerve root are much less common than those involving C2, but they are di- rectly related to the VA and often severely compressive. At this level, meningiomas with an extradural component are excep-

TABLE 1. Origins of Intermittent Compression of V3 in Authors' Series

Level

Pathology C0-C1 C1 -C2

Bone malformations Supplementary codyle 3 0 Klippel Feil 0 1 Joint anomaly 0 2

Infections Tuberculosis 1 0

Nerve C2 nerve root 0 1

tional. 24,26,27 They typically harbor invasive features to the sheaths of nerves and vessels. However, while they often invade the periosteal sheath of the VA, they respect the arterial wall.

Tumors originating from the soft tissues include different pathologies that tend to develop from the dura mater (Fig 5). 24,28 They may be benign (histiocytofibroma, angiomyoli- poma) or malignant (sarcomas of various types).

Bone tumors raise the problem of differentiating benign from malignant tumors (Figs 6 - 8 ) and tumors from pseudotumors (rheumatoid arthritis, other inflammatory processes, infections such as tuberculosis or parasitosis). It is often difficult to iden- tify a lesion that appears very destructive on the CT and MRI. The most common primary bone tumors at V3 are chordomas (Fig 9) followed by plasmocytomas, aneurysmal cysts, and os- teoid osteomas. However, metastases predominate over any type of primary bone tumor and are mostly related to lung and breast cancer. 24

With the notable exception of neurinomas, tumors at V3 often encase the VA and raise questions about preserving the artery during their resection. Although these tumors seldom extend beyond the periosteal sheath of the VA, it is wise to .perform a balloon occlusion test before they are resected. We have never had to ligate the VA because of dissection problems. In two of our patients, the VA was torn when the tumor was separated from it. The artery was repaired with one or two

SURGERY AROUND THE CRANIOCERVICAL JUNCTION 5 1

Page 3: The V3 segment of the vertebral artery: Surgery around the craniocervical junction

Fig 2. Intermittent compression of the V3 segment level in an 11-year-old boy. (A) Angiogram of the head while straight. (B) When the head is rotated to the left side, the VA is interrupted at the C1-C2 (arrow). (C) Axial MRI shows multiple cerebellar infarcts.

5 2 GEORGE, BLANQUET, AND ALVES

Page 4: The V3 segment of the vertebral artery: Surgery around the craniocervical junction

Fig 3. Bilateral extrinsic compression of the VA by a tuber- culous abscess of the atlas with severe stenosis on one side and complete occlusion on the other side. The patient was referred for treatment after experiencing five transient isch- emic attacks. Reproduced with permission from George B, Laurian C: The Vertebral Artery: Pathology and Surgery. New York, Sprintjer-Verlag, 1987, p 258

stitches. In five patients, the VA was sacrificed to achieve a radical resection of malignant tumors (mostly chordomas). One of these five patients poorly tolerated the balloon occlusion test, and a by-pass had to be performed with distal implantation of a venous graft on the VA above the arch of atlas. In the others, the VA was ligated and resected without revascularization.

Surgical Technique (Figs 10 and 11)

Much like surgery for tumors at V2, the VA must be controlled proximal and distal to the tumor. Proximal control is always possible, but distal control sometimes is difficult. The tumor carl fill the field up to the occipital bone and preclude control of the VA at the level of the foramen magnum. It has never been considered useful to open the dura to control the VA in the posterior fossa in order to control the artery distal to an extra- dural tumor.

The complex course of the VA from the C3 to the C1 trans- verse process makes exposure of the VA at this level difficult

even under normal conditions. If a tumor is developed at this level, control of the VA often starts proximally at the level of the C3 transverse process by unroofing the transverse foramen of C3.

When possible, the VA is controlled at C1-C2 or above the posterior arch of C]. If the transverse process of C2 or the C2-C3 segment is involved, it is safer to start from inferior or superior to this level and to progress superiorly, inferiorly, or both toward this point.

At V3, the nerve roots represent few difficulties because the C], C2, and C3 nerve roots have only a sensory territory. Their division leads to a sensory deficit in a very limited territory because there are connections among all the branches of the superficial nervous plexus and their territories overlap. The C2 root often must be divided to expose the C1-C2 segment of the VA, and its main branch is cut under the skin in the surgical approach.

When possible, the sympathetic chain must be controlled and preserved, but Horner's syndrome after injury of the sym- pathetic chain at the level of V3 is exceptional.

Control of the VA permits the main vascular tumoral feeders to be coagulated and divided. At V3 the anterior radiculomed- ullary artery is not a concern because it never arises above the level of C3. Therefore, the VA can be mobilized or transposed when necessary without fear of stretching the artery.

The anterolateral approach is used in most cases (Figs 10, 1 1, and 12, Table 3). 28 It permits the VA to be controlled and separated from the tumor or compressive element. It allows the different tumoral extensions to be followed (Fig 13): anteriorly into and before the anterior arch of atlas; posteriorly into and behind the posterior arch of atlas; inferiorly into and along the cervical spine; superiorly to the occipital bone and the jugular foramen; and medially into the spinal canal extra- or intra- durally following the nerve roots. The posterolateral approach offers fewer possibilities for following tumoral extensions ex- cept intradurally inside the posterior fossa and spinal canal. 24,28 Therefore it is reserved for small tumors located at the posterior part of the bone and the extradural space of the craniocervical junction or for tumors whose main bulk is intradural and ex- tending more or less extradurally (eg, meningiomas and some neurinomas).

Control of the VA to Improve Surgical Access:

Intradural Foramen Mclgnum 24,26,27.29~33 (Figs 1 4 and 15). At C1, the VA runs horizontally in a groove and then obliquely

TABLE 2. Types of Tumors Compressing V3 in Authors' Series

Tumor (N = 114) No.

Neurinoma 32* Meningioma 3 Hemangiopericytoma 1 Chordoma 30 Sarcoma 16 Plasmocytorna 4 Osteochondroma 2 Osteoid Osteoma 7 Aneurysmal cyst 3 Fibrous dysplasia 3 Metastasis 15 Histiocytosis 2 Others 21

*Of 32 neurinomas, 15 were extradural and 17 were intra- and extradural.

SURGERY AROUND THE CRANIOCERVICAL JUNCTION 5 3

Page 5: The V3 segment of the vertebral artery: Surgery around the craniocervical junction

Fig 4. (A) MRI without (upper) and with (lower) contrast injection shows an hour-glass neurinoma of the C2 nerve root. (B) Operative exposure (left side) of an hour-glass neurinoma through a posterolateral approach. T = tumor. Black star = VA. Open star = C1 nerve root. The VA is elevated out of the atlas groove. The arrow indicates the end of the groove. 1 = posterior arch of atlas. 2 = lamina of C2. Reproduced with permission from Donald PJ (ed): Manage- ment of the Vertebral Artery in Surgery of the Skull Base. Philadelphia, Lippincott-Raven, 1998, pp 533-553.

superiorly and medially to reach the dura. The VA pierces the dura at the midpoint of its lateral aspect. Running in the sub- arachnoid space, it passes in front of the medulla oblongata. By following the course of the VA, the space in front of the neuraxis can be reached (Figs 14 and 15). Any tumoral process that develops anterior or lateral to the neuraxis displaces the neuraxis so that the space in front of or lateral to it is enlarged (Fig 16). By using these two elements (location of the VA and displacement of the neuraxis), the anterior and lateral sub- arachnoid space at the level of the foramen can be approached magnum. The anterolateral approach can be used, but the pos- terolateral approach is a better option (Table 3) (Fig 17). Re- gardless of surgical approach, drilling the important bony structures of the two joints C0-C1 (occipital condyle-lateral mass of atlas) and C1-C2 should be avoided or minimized. 34

The exposure is modified according to the exact location of the tumor. Its location must be considered in terms of two parameters: the horizontal plane and the relationship to the VA. In the horizontal plane a tumor can be posterior, lateral, or anterior. An anterior tumor is located on the anterior midline and displaces the neuraxis straight posteriorly. A lateral tumor is lateral to the anterior midline and displaces the neuraxis more or less obliquely laterally and posteriorly (Figs 17 and 18). Consequently, lateral tumors retract the neuraxis laterally and the surgical approach does not need to be enlarged exten- sively in that direction. Conversely, anterior tumors do not push the neuraxis toward the opposite side. The surgical open- ing must be extended up to the occipital condyle and lateral mass of atlas to be able to move around the neuraxis. There is no need to resect any part of these bony elements because the

posterior displacement of the neuraxis by the tumor enlarges the space anterior to it and widens the access along the VA.

The relation between the tumor and the VA modifies the level of opening. A tumor located above the VA requires the field above the VA to be enlarged (ie, toward the occipital condyle). A tumor located below the VA requires the field below the VA to be enlarged (ie, toward the lateral mass of atlas). Then the dura is opened vertically slightly lateral to midline and curved later- ally at both extremities. A contraincision is made horizontally toward the VA and above or below the VA according to the location of the tumor above or below the VA, respectively. When tumor extends on both sides of the VA, the dura is cut toward the VA and then around it at the point where it pierces the dura. This maneuver can be difficult because the dura and the VA periosteal sheath invaginate a few millimeters around the VA. Opening the dura around the VA is even more difficult in case of meningiomas that insert at this point.

The main vascular feeder of foramen magnum meningiomas is the anterior meningeal artery, which arises from the C2-C3 portion of the VA. Consequently, it is always a good option to start resecting the meningiomas at the inferior pole. In the case of a neurinoma, the main vascular feeder arises from the first radicular artery exiting the VA in the groove of atlas for the C1 nerve root and from the second radicular artery exiting the VA between the C1 and C2 transverse processes for the C2 nerve root.

The most common pathologies at the level of the intradural foramen magnum are meningiom.as followed by neurinomas and various types of tumors such as epidermoid cysts, heman- gioblastomas of the C1 root, or neurenteric cysts (Table 4) . 24

54 GEORGE, BLANQUET, AND ALVES

Page 6: The V3 segment of the vertebral artery: Surgery around the craniocervical junction

Fig 5. Extradural benign tumors. (A) Coronal MRI of a neurinoma. (B) Axial CT scan of an angiomyolipoma. (C) Axial MRI and (D) angiogram of an histiocytofibroma.

SURGERY AROUND THE CRANIOCERVICAL JUNCTION 5 5

Page 7: The V3 segment of the vertebral artery: Surgery around the craniocervical junction

Fig 6. Osteoid osteoma of the right occipital condyle. Axial CT scan before (A) and after (B) surgical resection.

56 GEORGE, BLANQUET, AND ALVES

Page 8: The V3 segment of the vertebral artery: Surgery around the craniocervical junction

Fig 7. Axial CT scans of three different lesions with destruc- t ive features of the bone. (A) Metastasis, (B) aneurysmal cyst, and (C) tuberculosis.

SURGERY AROUND THE CRANIOCERVICAL JUNCTION 5 7

Page 9: The V3 segment of the vertebral artery: Surgery around the craniocervical junction

Fig 8. (A) Sagittal and (B) axial MRIs showing an aneurysmal cyst involving the Cl and C2 vertebrae and encasing both VAs (arrows). Surgical resection was achieved in one stage through bilateral anterolateral and posterior approaches with occipitocervical bone grafting and halo fixation.

~8 GEORGE, BLANQUET, AND ALVES

Page 10: The V3 segment of the vertebral artery: Surgery around the craniocervical junction

Fig 9. A chordoma (T) of the C1 and C2 vertebrae encasing the VA (black Star) on one side was resected through antero- lateral approach. (A) Preoperative sagittal MRI, (B) postop- erative sagittal CT scan, (C) preoperative coronal MRI, and (D) postoperative CT scan.

SURGERY AROUND THE CRANIOCERVICAL JUNCTION 59

Page 11: The V3 segment of the vertebral artery: Surgery around the craniocervical junction

Fig 10. Osteoblastoma of the occipital condyle seen on (A) axial CT scans at the level of C l and (B) at the level of the occipital condyle. (C) Coronal CT scan, T = tumor. Black star = VA. Surgical exposure and resection (left side). (D) Opening the surgical field. The sternomastoid muscle (1) is detached from the mastoid process. The digastric muscle (2) is exposed at the upper part of the field. (E) The internal jugular vein (3) and the spinal accessory nerve (4) are exposed. The tip of the transverse process of the atlas (5) with small muscles attached on it are visible. The fat pad (6) covering these muscles has been dissected free and rolled around the spinal accessory nerve. (F) The small muscles have been detached from the tip of the transverse process of the atlas (5) showing the two parts of the V3 segment of the VA (black stars).

6 0 GEORGE, BLANQUET, AND ALVES

Page 12: The V3 segment of the vertebral artery: Surgery around the craniocervical junction

Fig 10. (Continued). (G) The transverse foramen of atlas (open circle) has been opened. The blade protects the internal jugular vein and the spinal accessory nerve. The bone tumor (T) is covered by inflammatory tissues. (H) The distal part of the posterior arch of the atlas has been resected. The bone tumor has been drilled off working on both sides of the superior C1 portion of the VA. A residual bone cavity is visible (asterisk).

carot T; L Int. ju ....

C . Mastoid _

~ '~aransverse

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~ , : . i . , ~ , ~ ~ - _ ? Strippe d - ~ ~ periosteum

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Fig 11. Schematic drawings of the steps of the anterolateral approach. (A) Surgical positioning and skin incision. The head is markedly turned toward the opposite side to bring the posterior part of the craniocervical junction into view. (B) Opening the surgical field between the internal jugular vein and the sternomastoid muscle. (C) Detachment of the small muscles from the transverse process of the atlas exposes the two portions of V3. (D) The VA is dissected extraperiosteally to keep the periosteal sheath enclosing the venous plexus intact. At the level of the C1 transverse foramen, the spatula split the periosteum from the bone. (E) A Kerrison rongeur is pushed between the bone and the periosteum to open the transverse foramina of C1 and C2.

Page 13: The V3 segment of the vertebral artery: Surgery around the craniocervical junction

Fig 12. Extended posteriorly, the anterolateral approach ex- poses the dura mater of the craniocervical junction. (A) First step of surgical exposure (left side). (B) After resection of the posterior arch of atlas and opening of the posterior fossa. 1 = Internal jugular vein. 2 = spinal accessory nerve. 3 = digastric muscle. 4 = Fat pad. 5 = Tip of C1 transverse process. Black star = VA. Asterisk = Posterior arch of atlas. Circle = C2 nerve root. D = Dura mater.

Extradural lesions that protrude intradurally (eg, synovial cysts) can be removed through the posterolateral approach (Fig 19). This approach also is used for tumors or lesions (cavernous angiomas) of the anterior or lateral part of the medulla oblon- gata and for aneurysms of the VA or the posterior inferior cerebellar artery.

Jugular Foramen; the Juxtacondylar Approach 35. As it is well demonstrated on a coronal view of an MRI or CT scan (Fig 20), the jugular foramen projects exactly above the transverse fora- men of atlas. Consequently, moving vertically from the VA in the transverse process of C1 along the condyle leads to the inferior aspect of the jugular foramen.

The anterolateral approach is performed as previously de- scribed (see "Surgical Exposure") to expose the transverse pro- cess of C1 followed by the C1-C2 and the superior C1 segments of the VA. The transverse process of the atlas is resected and the C1 foramen is opened. The VA is exposed from C2 to the

TABLE 3. Numbers of Surgical Approaches Performed at V3 for 230 Pathological Entities in Authors' Series

Surgical Approach

Anterolateral Posterolateral

Extradural tumors (N = 116) 64 52 Intradural tumors (N = 92) 2 90 Non tumoral process (N = 22) 12 10

62

foramen magnum (Fig 21). It seldom must be mobilized from the transverse foramen of C1. The lateral part of the occipital bone and part of the mastoid process are resected to expose the distal part of the sigmoid sinus. At this point only a small piece of bone corresponding to the jugular tubercle remains between the end of the sigmoid sinus and the beginning of the internal jugular vein. By drilling the jugular tubercle, posterior and inferior portions of the jugular foramen are opened. 35

This approach is sufficient to expose and remove tumors located in the jugular foramen, typically neurinomas (Fig 22, Table 5). The lower cranial nerves (IX, X, XI, and XII) are controlled in the retropharyngeal space and followed into the jugular foramen. This technique almost always makes it possi- ble to identify the nerve or the part that gives rise to neurino- mas. Thus it is possible to preserve the nerves that are not involved in the tumor. An intradural extension can be reached by opening the dura of the posterior fossa across the end of the sigmoid sinus. This maneuver avoids drilling the petrous bone; a partial mastoidectomy is sufficient.

When the tumor extends beyond the jugular foramen into the petrous bone, the juxtacondylar approach, which requires extensive drilling of the petrous bone, is used (Fig 23) (com- bined juxtacondylar and infratemporal approaches or com- bined juxtacondylar and one type of transpetrosal approach). This approach is used most commonly to reach paragangliomas (glomus jugulare tumors). The juxtacondylar approach re- duces a considerable amount of petrous bone drilling. If the

GEORGE, BLANQUET, AND ALVES

Page 14: The V3 segment of the vertebral artery: Surgery around the craniocervical junction

~AL

PL

Fig 13. (A) Schematic drawing of the possible extensions of the anterolateral (AL) and posterolateral (PL) approaches in the axial plane. (B) Postoperative axial CT scan at the foramen magnum showing the bone resection from the anterior midl ine to the poster ior midl ine achieved through an anterolateral approach to remove a chordoma.

Fig 14. Cadaveric dissect ion view of the posterolateral approach after dural opening (right side). The dura mater has been cut around the VA. (A) Lower part of the foramen magnum. The spatula separates the VA from the C1 nerve root, Black star = VA, 1 = C l nerve root. 2 = C2 nerve root. D = Dura mater, 3 = Denticulate l igament. (B) Upper part of the foramen magnum, The spatula and the sucker elevate the cerebel lum to show the vagus nerve. D = Dura mater. Black star = VA. 1 = spinal accessory nerve. 2 = C2 nerve root. 3 = Denticulate l igament, The f i rst arch around the VA has been cut,

SURGERY AROUND THE CRANIOCERVICAL JUNCTION 6 3

Page 15: The V3 segment of the vertebral artery: Surgery around the craniocervical junction

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XI Fig 15, Schematic drawings of the different steps of the posterolateral approach, (A) Skin incision, (B) Exposure of the left side. The spatula elevates the periosteum of the groove of the atlas to preserve the periosteal sheath of the VA. (C) Resection of the posterior arch of atlas up to but not including the occipital condyle and the lateral mass of the atlas. Notice the gain of exposure given by the posterolateral approach compared to the standard midline approach. (D) Dural incision (dotted line), Notice the contra-incision di- rected toward the VA, (E) Opening the dura shows the normal anatomy of the foramen magnum.

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Fig 16. Schematic drawing of the exposure of the foramen magnum region through the posterolateral approach showing the (A) undisturbed anatomy, (B) a lateral meningioma, and (C) anterior meningioma. Notice the displacement of the neuraxis-- straight posteriorly for the anterior tumor and posterolateral for the lateral tumor. A laterally located tumor is easily accessed without drill ing the occipital condyle or lateral mass of the atlas. For an anteriorly located tumor, the access is more narrow. Limited drill ing of the lateral mass of atlas, occipital condyle, or both may be needed. (D) Axial MRI view of undisturbed anatomy and (E) axial CT scan after resection of an anterior meningioma through a left postero-lateral approach.

SURGERY AROUND THE CRANIOCERVICAL JUNCTION 6 5

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Fig 17. Anterior meningioma resected through the posterolateral approach (left side). Axial MRI view before (A) and after (B) surgical resection. Sagittal MRI before (C) and after (D) surgical resection.

6 6 GEORGE, BLANQUET, AND ALVES

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Fig 17 (continued). (E) Exposure of C1 posterior arch (1) and lamina of C2 (2). Black star = VA. Black circle = C2 nerve root. (F) The poster ior fossa has been opened and the pos- ter ior arch of the atlas has been resected. Black star = VA. Black circle = nerve root. 1 = lateral mass of atlas. (G) Dural opening showing the tumor (T). Black star = VA. Black circle = C2 nerve root. (H) Operative f ield after surgical resection. Black star = VA. Black circle = C2 nerve root. The intradural port ion of the C2 nerve root and VA is crossed by the medul lary root of the spinal accessory nerve (open star). Asterisk = Cerebellum. Reproduced wi th permission from Donald PJ (ed): Management of the Vertebral Artery in Sur- gery of the Skull Base. Philadelphia, Lippincott-Raven, 1998, pp 533-553.

SURGERY AROUND THE CRANIOCERVICAL JUNCTION 6 7

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Fig 18. (A) Axial and (B) sagittal MRIs showing a lateral meningioma resected through the posterolateral approach. (C) Extradural exposure (right side) showing the VA (black star), the occipital condyle (black circle), and the lateral mass of atlas (asterisk). (D) Intradural exposure. T = Tumor. Black star = VA. The dura mater is cut on both sides of the VA. Black circle = C2 nerve root. Open star = spinal accessory nerve. Reproduced with permission from Donald PJ (ed): Management of the Vertebral Artery in Surgery of the Skull Base. Philadelphia, Lippincott-Raven, 1998, pp 533-553.

6 8 GEORGE, BLANQUET, AND ALVES

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Fig 19. Sagittal MRI of a synovial cyst (white star) protruding intradurally. The cyst was resected through the posterolat- eral approach.

fallopian canal is intact, it is not opened and the facial nerve is kept in place protected by its bony canal. Likewise, the inner ear, if not invaded, can be preserved. When possible, the lower cranial nerves are also better preserved through this approach. The vertical and horizontal segments of the petrosal portion of the carotid artery can be controlled by working alternatively above and below the fallopion canal. This technique provides control of the-tumor's vascular feeders arising from the VA which is obtained by exposure of the VA. Finally, the cranio- cervical junction remains stable because the two joints (C0-C1 and C1-C2) are preserved. Some paragangliomas extend into the occipital condyle but not so far that stability is compro- mised.

TABLE 4. Types of Foramen Magnum Tumors (Intradural Tumors, N = 92) in Authors' Series

Tumor No.

Meningioma 72 Neurinoma 21 Hemangioblastoma 3 Epidermoid cyst 4 Ependymoma 1 Neuroenteric cyst 1

*Of 21 neurinomas, 4 were intradural and 17 were intra- and extradural.

Anterior Portion of the CraniocervicaI Junction 28,3<38 (Figs 24, 25, 26). Through the anterolateral approach, the anterior por- tion of the craniocervical junction can be reached: the tip of the clivus, the anterior arch of atlas, and the odontoid (Figs 24, 25, and 26). After V3 is exposed through an anterolateral approach, the transverse process of atlas is resected and the C1 transverse foramen is opened. The VA is transposed posteriorly and me- dially after it has been mobilized out of the foramen. Dissection proceeds behind the pharynx and neurovascular elements and in front of or into the anterior arch of the atlas. If tumor invades the bone, the route is the shortest way because drilling is min- imized. Pseudotumors such as bony malformations (odontoid malposition or invagination) or inflammatory processes (rheu- matoid arthritis) also can be treated through this approach (Table 6). 36

Typically, a considerable amount of C0-C 1 or C 1-C2 must be drilled and a fixation procedure becomes necessary. Typically, the stability of the craniocervical junction has already been compromised by the tumoral destruction or the pseudotumoral process. Surgery of the craniocervical junction requires deter- mining the likelihood of instability before surgery rather than after it. The stability of the craniocervical junction may be compromised by the pathological process but never by the surgical drilling.

Fixation can be achieved in two ways (Table 7). The first is the standard technique of occipitocervical fusion with one of the many available instrumentation systems and bone grafts. The other technique, lateral grafting, is per- formed through the same anterolateral approach as used to remove the lesion. 28,37 An iliac bone graft is placed between the remaining upper portion of the lateral wall of the craniocervical junct ion (jugular tubercle, occipital con- dyle, or both) and the C2 or C3 vertebral body (Fig 25). A plate can be screwed between the occipital bone and lamina of C2. Plating, however, is not mandatory. Of the 7 cases in which we have used this technique, plating was needed only once.

Fig 20. Coronal CT scan of a jugular foramen schwannoma showing the lateral wall of the craniocervical junction. 1 = Jugular tubercle. 2 = Occipital condyle. 3 = Lateral mass of atlas. 4 = C2 facet. T = tumor. Notice the proximity of the VA (black star) to the inferior portion of the tumor and the jugular foramen.

SURGERY AROUND THE CRANIOCERVICAL JUNCTION 6 9

Page 21: The V3 segment of the vertebral artery: Surgery around the craniocervical junction

A ~-. \ ~ m ~ ~ S igmoid sinus

~ . '

Dural incision- and division of sinus

E

C Sigmoid sinus

Hypoglossal n. (Xll)

Fig 21. (A) Schematic drawing of the VA transposit ion (not always necessary) and drilling of the jugular tubercle. The lateral part of the posterior fossa has been opened to expose the sigmoid sinus. (B) In the corresponding cadaver dissection, the Cl transverse foramen has been opened, but the VA (black star) has not been transposed. The sigmoid sinus (1) and jugular bulb (2) are exposed but still covered by a shell of bone. 3 = Internal jugular vein. D = Dura mater of the posterior fossa. (C) Schematic drawing shows the full exposure of the venous axis. (D) In this "Cadaver" dissection, the venous axis has been opened longitudinally. Sigmoid sinus (1), jugular bulb (2) and internal jugular vein (3). Notice the VA: black star; cranial nerves IX, X, and XI nerves (asterisk); and the internal carotid artery (open circle). (E) In this schematic drawing, the dura mater has been opened across the distal part of the sigmoid sinus bringing into view the intradural part of the lower cranial nerves. (F) Corresponding cadaveric dissection. Black star = VA. Asterisk = lower cranial nerves. C = internal carotid artery. Through the dural opening (stitches), note the intradural port ion of the nerves (asterisk) and the posterior inferior cerebellar artery.

7 0 GEORGE, BLANQUET, AND ALVES

Page 22: The V3 segment of the vertebral artery: Surgery around the craniocervical junction

TABLE 5. Types of Jugular Foramen Tumors (Juxtacondylar Approach, N = 72) in Authors' Series

Tumor No.

Paraganglioma 51 Neurinoma 11 Meningioma 3 Sarcoma 5 Histiocytofibroma 1 Histiocytosis 1

Fig 22. First step of exposure (right side) of a jugular fora- men tumor with control of the VA (black star). The internal jugular vein (black circle) is fi l led with tumor. Internal carotid artery (open circle). Cranial nerves XII (1), X (2), and XI (3).

Fig 23. Jugular foramen paraganglioma (left side). (A) Exposure of the jugular foramen through the juxtacondylar approach. Black star = VA. T = tumor in the jugular foramen. D = dura of the cerebellum. Open circle = Internal carotid artery. The internal jugular vein has been ligated and divided (not visible). The sigmoid sinus has been occluded by Surgicel packing (not visible). M = Mastoid process. Black circle = Digastric muscle. Asterisk = Fat pad around the spinal accessory nerve. (B) Same case after the tumor has been resected through combined juxtacondylar and infratemporal approaches. Black star = VA. star. Asterisk = lower cranial nerves and internal carotid artery. 7 = labyrinthine bloc and VII cranial nerve.

Fig 24. Cadaver dissection IC of the anterolateral approach (left side). Exposure of the odontoid process (asterisk) with the spatula on the tip. The lateral mass of atlas has been drilled off between the facet of the occipital condyle (black circle) and the facet of the C2 vertebra (open circle). The VA has been transposed posteriorly (bottom of the picture but not visible).

Fig 25. Operative view (left side) of a lateral graft for f ixation after a bone tumor has been removed. Black star = VA. 2 -- C l -C2 VA segment. Asterisk = bone graft.

SURGERY AROUND THE CRANIOCERVICAL JUNCTION 71

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Fig 26. Pseudotumor at C1-C2. (A) Sagittal MRI and (B) Sagittal CT scan before treatment, (C) Sagittal and (D) axial CT scans after surgical decompression and lateral grafting. Black circle = iliac bone graft.

7 2 GEORGE, BLANQUET, AND ALVES

Page 24: The V3 segment of the vertebral artery: Surgery around the craniocervical junction

G

Fig 26. (Continued). (E) Lateral approach (right side) with exposure of the C1-C2 joint (1, 2). (F) The lateral mass of atlas has been drilled out. (G) Lateral graft has been placed. Black circle: iliac bone graft. Black star = VA. N = spinal accessory nerve. J = Internal jugular vein.

TABLE 6. Types of Nontumoral Pathology (N = 22) at the Craniocervical Junction and Surgical Approach in Authors' Series

Surgical Approach

Anterolateral Posterolateral Total

Bone malformation 5 6 11 Infectious process 2 - - 2 Synovial cyst 1 1 2 Inflammatory ,process 2 3 5 Degenerative process 2 - - 2

TABLE 7. Fixation Procedures Used to Treat 230 Pathological Entities at the Craniocervical Junction in Authors' Series

Lesion

Fixation Technique

Occipitocervical fixation Lateral grafting

Extradural tumors (n = 116) 19 5

Intradural tumors (n = 92) - - - -

Nontumoral process (n = 22) 5 2

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extrinsic lesions. Neurosurgery 24:206-214, 1989 2. Bauer RB: Mechanical compression of the vertebral arteries in Ber-

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4. Morimoto T, Kaido T, Uchiyama Y, et al: Rotational obstruction of �9 nondominant vertebral artery and ischemia. J Neurosurg 85:507-509, 1996

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9. Hardesty WH, Whitcare WB, Toole JF, et al: Studies on vertebral artery blood flow in man. Surg Gynecol Obstet 116:662-664, 1963

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11. Barton JW, Margolis MT. Rotational obstruction of the vertebral artery at the atlanto-axial joint. Neuroradiology 9:117-120, 1975

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vertebral artery occlusion from a fibrous band. Case report. J Neu- rosurg 56:581-583, 1982

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17. Takakuwa T, Hiroi S, Hasegawa H, et al: Os odontoideum with vertebral artery occlusion. Spine 19:460-462, 1994

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20. Ford FR: Syncope, vertigo and disturbances of vision resulting from intermittent obstruction of the vertebral arteries due to defect in the odontoid'process and excessive mobility of the second cervical vertebral. Bull Johns Hopkins Hosp 91:168-173, 1952

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30. Market JM, Chandler WF, Deveikis JP, et al: Use of the extreme lateral approach in the surgical treatment of an intradural ventral cervical spinal cord vascular malformation: Technical case report. Neurosurgery 38:412-415, 1996

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32. Spinnato S, Talacchi A, Musumeci A: Dumbbell-shaped hypoglossal neurinoma: Surgical removal via a dorsolateral transcondylar ap- proach. A case report and review of the literature. Acta Neurochir (Wien) 140:827-832, 1998

33. Bertalanffy H, Seeger W: The dorsolateral, suboccipital, transcondy- lar approach to the lower clivus and anterior portion of the cranio- cervical junction. Neurosurgery 29:815-821, 1991

34. Lot G, George B: The extent of drilling in lateral approaches to the craniocervical junction area from a series of 125 cases. Acta Neuro- chir (Wien) 141:111-118, 1999

35. George B, Lot G, Tran Ba Huy P: The juxtacondylar approach to the jugular foramen (without petrous bone drilling). Surg Neurol 44:279- 284, 1995

36. AI-Mefty O, Borba AB, Aoki N: The transcondylar approach to extradural nonneoplastic lesions of the craniovertebral junction. J Neurosurg 84:1-6, 1996

37. Bongiovanni F, Assadurian E, Polivka M: Aneurysmal bone cyst of the atlas. Operative removal by an anterolateral approach. A case report. J Bone Joint Surg 78:1574-1577, 1996

38. Crockard A: Surgery for anteriorly placed meningiomas at the fora- men magnum in meningiomas and their surgical management. HH Schmidek (ed), W.B. Saunders Co, Philadelphia, PA, 1991, pp 471- 479

7 4 GEORGE, BLANQUET, AND ALVES


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