Compression of and by the Vertebral Artery

Bernard George, MD, and Alexandre Carpentier, MD

The vertebral artery (VA) may be either intermittently or perma- nently compressed by different factors. Intermittent compres- sions are generally due to bony, ligamentous, or muscular anom- alies or pathologies that require surgical treatment only when causing compression. They cause compression only during par- ticular movements of the head and neck. Surgery must be pursued only if the same movement that produces symptoms also severely compresses the VA during dynamic angiography. Intermittent compressive factors typically include sympathetic elements in the first segment, osteophytic spurs and fibrous bands in the second segment, and rotational obstruction (bow hunter's syndrome) and C1-C2 instability in the third segment. Treatment must include resection of the compressive factor and opening of the adjacent transverse processes. A fusion proce- dure is performed in the case of instability. Permanent compres- sion tends to be related to the development of tumors, but is also exceptionally symptomatic when due to occlusion. The VA may also be responsible for neurovascular compromise of the spinal cord or nerve roots. The cause is either tortuosity or congenital malformation (intradural course) of the VA. Copyright �9 2001 by W.B. Saunders Company

M any different factors, including osteophytes, fibrous

. bands, extreme rotation, dislocation, trauma, nerves, and bony malformations, can compress the vertebral artery (VA). Most of these extrinsic factors produce intermittent occlusion of the VA during particular movements. Conversely, variations in the course of the VA may compress the spinal cord or spinal nerve roots, causing neurovascular compromise similar to those underlying trigeminal neuralgia.

Extrinsic Compression of the VA

Symptoms and Signs

In most cases, symptoms related to extrinsic compression of the VA are subjective and intermittent. Patients often report a long history of repetitive symptoms of vertebrobasilar insufficiency, including dizziness, gait disturbance, blurring of vision, diplo- pia, limb paresthesias, and tinnitus. 1,2 These symptoms are intermittent, lasting a few seconds or minutes during a partic- ular movement and resolving soon after the movement is stopped, On patient presentation, the neurological exam is nor- mal with the head and neck in a neutral position or reveals minor symptoms such as nystagmus or slight ataxia. However,

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

Address reprint requests to Bernard George, Department of Neurosur- gery, H6pital Lariboisiere, 2, rue Ambroise Par6, 75010 Paris, France. E-mail: bernard.george@lrb.ap-hop-paris.fr

Copyright �9 2001 by W.B. Saunders Company 1092-440X/01/0404-0005535.00/0 doi:l 0.1053/otns.2001.30170

when the patient places his head in a position known to pro- duce symptoms, the physician may observe the symptoms.

In a few cases, especially those associated with infarction demonstrated on magnetic resonance (MR) imaging, clear signs of brain stem, cerebellar, or occipital lobe dysfunction are dem- onstrated.3,4, ~

Imaging

Computed tomography (CT) and MR imaging must be per- formed on the brain and cervical spine. In a few cases, infarcts in the vertebrobasilar territory may be discovered. 3,4,5 Spinal cord swelling with a small infarct remaining 3 months after the onset of symptoms has been reported in one case. 4

CT and MR angiography permit investigation of the four main vessels (the carotid and vertebral arteries) in the neck and in the brain. At present, they cannot replace dynamic angio- graphic studies, but they give valuable information on the size of vessels, especially the diameters of both VAs and of both posterior communicating arteries. This information is invalu- able for assessing compensation by the collateral pathways.

Three-dimensional (3D) CT angiography should be per- formed more often because it allows a better understanding of the relationship between bone structures and the VA and of the mechanism of VA compression. 6,7

Traditional angiography is still necessary but must be per- formed on both VAs. It must be a dynamic study with anglo- graphic series in the neutral position and in the head and neck position that produces symptoms. Some authors perform the angiography with various degrees of head and neck movement, for example, with rotation at 45, 60 and 90 degrees. 8 In some cases, it is useful to study the different components of the head and neck movement separately, most commonly rotation and extension, and then to study them in combination.

Treatment

Treatment should be considered only when extrinsic compres- sion of the VA has been clearly demonstrated. First, similar symptoms of vertebrobasilar insufficiency or ischemia must be reported each time the patient moves his head in the same way. Second, the same head and neck position as the one inducing symptoms must be reproduced during the angiographic study and must be associated with severe stenosis or occlusion of the VA (Fig 1). Finally, the collateral pathways must fail to com- pensate for reduced blood flow. Collateral flow may compen- sate for the affected VA, which may be hypoplastic or atretic, or show atherosclerotic stenosis. 2 When visual disturbances sug- gest occipital lobe dysfunction, the posterior communicating arteries should not fill the territory of the posterior cerebral arteries. 8 There are a few exceptions-contralateral VAs of equal size have been reported. A paradoxical case has been reported in which the affected VA was atretic, ending at the posterior inferior cerebellar artery. 7 In the case of occlusion of an atretic

2 0 2 Operative Techniques in Neurosurgery, Vol 4, No 4 (December), 2001: pp 202-218

high risk of hemorrhagic complications. Cervical traction may be offered to reduce subluxation with a locked facet.

Surgical options attempt to solve the problem in different ways. Spinal fixation suppresses the responsible movement and therefore the VA compression and associated symptoms. Spinal fixation may be acceptable for one or two vertebral levels in- volving the V2 segment. Involvement of V3, however, severely reduces the possibilities of head rotation. Therefore, spinal fixation is a good solution only in cases of dislocation, which would be treated by spinal fixation anyway. Bypass using a saphenous vein graft anastomosed proximally to the common carotid artery and distally to the VA distal to the level of com- pression can be considered when the VA cannot be decom- pressed or is already definitively occluded (Fig 2).2~ A bypass sometimes avoids the difficulty of separating the VA from the compressive agent but is associated with potential complica-

Fig 1. Angiographic study with the head in neutral position (A) and rotated toward the opposite side (B). Complete dis- appearance of contrast at C6 where the VA enters the trans- verse canal. At surgery (C) a fibrous thickening of the Iongus colli and scalenus muscle was discovered. Notice the bayo- net-shaped course of the VA (black star), The tip of the forceps is on the opened transverse foramen.

VA, no compensation can be obtained from the opposite VA because the.vessels do not join at the origin of the basilar trunk (see Surgical Anatomy). As a consequence, the symptoms can only correspond to the posterior inferior cerebellar artew ter- ritory: Wallenberg's syndrome or vermian cerebellar syndrome. Most extrinsic VA compressions decrease the arterial flow of the vertebrobasilar system, but an embolic mechanism may also be the cause of the symptoms. Complete occlusion with prox- imal thrombosis due to extrinsic compression may be respon- sible for distal embolism. This mechanism is commonly ob- served in trauma 9 but has also been reported in osteophytic compression. ~~ Repetitive compression of the VA would cause intimal damage and dissecting hematoma or favor prox- imal blood stasis.

Once the diagnosis is established, several therapeutic options can be contemplated. Many treatments have been reported: verbal recommendations to avoid the symptom-producing movement, 1~ anticoagulant therapy, 16 cervical traction, 17 spi- nal fixation, 1,18,19 bypass, 20 and direct decompression. 2,5,21-26 Nonsurgical treatments are acceptable for elderly patients with minor symptoms. Anticoagulant therapy is a poor option. It is unacceptable to start such treatment in young patients for many years, and it is questionable in elderly patients because of the

Fig 2. Fibrous bands severely compress the VA at C6 and atherosclerotic stenosis is present at its origin. (A) Anglo- graphic view. (B) Intraoperative view of the treatment by saphenous vein graft (asterisk) between the common carotid artery (black circle) and the VA at Cl-C2.

COMPRESSION OF AND BY THE VERTEBRAL ARTERY 2 0 3

Fig 3. Cadaveric dissection showing the relation of the Cl-C2 portion of the VA (black stars) and the Cl -C2 joint. If the atlas (1) slides over C2 (2) too much, the VA is stretched and compressed by the C2 facet. Posterior arch of atlas: asterisk. Accessory nerve: arrow. (Reproduced with permis- sion from: Management of the Vertebral Artery in Surgery of the Skull Base. P. J. Donald (ed). Lippincott-Raven Pub. Philadelphia. New York. 1998. pp 533-553).

tions. In most cases, the best option is direct decompression of the VA.

Principles of Decompression

The VA must be exposed and controlled proximally and distally from the level of compression using the lateral approach. At the level of the V1 segment, control of the origin of the VA and of the subclavian artery may also be required. At the level of the V2 and V3 segments, the transverse processes above and below the com- pression must be exposed; then the foramina must be opened extraperiosteally to keep the periosteal sheath surrounding the VA and its venous plexus intact. Next, the different elements com- pressing the VA must be cut or resected. It is mandatory that the treatment include these two steps: (1) proximal and distal control of the VA with opening of the transverse foramina and 2) resection of the compressing elements. The case reported by Kawaguchi et al. demonstrates the necessity of these two surgical steps. Two surgeries were performed. In the first, the compressing elements, the tendons of the longus colli and anterior scalenus muscles, were divided from the transverse process of C6. A fat pad was interposed at the second surgery. The first surgery resulted in a brief (2 months) improvement, and the second surgery did not change the patient's condition. After a third operation in which the C4 and C5 transverse foramina were opened, the symptoms resolved. During intraoperative angiography, complete occlusion of the right VA during a 90 ~ rotation persisted after the offending osteophytes were removed but disappeared after the transverse foramina were opened. Matsuyama et al 6 compared the results of two groups of patients. The first group of 8 patients underwent a posterior fusion while the second group of 9 patients underwent decompression. The first group had complete relief from their preoperative symp- toms while only 6 of the 9 patients of the second group had complete relief. Symptoms recurred in the three remaining pa- tients, and dynamic angiography still showed a VA occlusion. Two patients underwent fusion and the third received anticoagulation therapy. Apparently, their decompression technique consisted of cutting the fibrous bands and did not include opening the trans- verse foramina.

VA Compressing Factors

V3 Segment

1) Physiological rotational obstruction (Fig 3). Several authors have demonstrated by dynamic angiography on cadavers and live patients that hyperextension and contralateral rotation may be responsible for complete occlusion of the VA at C 1-C2. This result was reported as early as 1927 by de Kleyn and Nieuwen- huyse. 27 Toole and Tucker reported a study on 20 cadavers perfused through the aorta under constant pressure. 28 In 18 cases, the rate of blood flow through one or both VA decreased to less than 10% of its initial rate when the head was flexed or extended less than 45 ~ , rotated less than 45 ~ , and bent laterally less than 30 ~ , values well within the range of normal head movement. Conversely, Brown and Tatlow 29 found complete occlusion of one VA in only 5 of 41 cases by rotating the head 90 ~ with the neck extended. Physiological compression of the distal cervical VA during head movement has also been shown angiographically in patients by angiography 1,3~ and by 3D CT. 33 Therefore, ipsilateral compression of the VA during con- tralateral rotation combined with another factor compressing the contralateral VA during the same movement would be likely to produce ischemic symptoms. Kawaguchi et al s re- ported a 56-year-old man with a subluxation of the C4-C5 apophypseal joint during ipsilateral rotation and contralateral VA occlusion at C1-C2 during the same movement. A similar mechanism may explain the symptoms that appear when a VA is smaller than or of equal size to the contralateral VA. In the

Fig 4. Angiogram showing the imprint of the C2 nerve root on the Cl -C2 portion of the VA (arrow). Notice another plicature of the VA at C4-C5 (arrow). (Reproduced with per- mission from: The Vertebral Artery. Pathology and Surgery. B. George, C. Laurian. Spdnger-Verlag. Wien. New York. 1987. p 258).

2 0 4 GEORGE AND CARPENTIER

Fig 5. Bony malformation in an 8-year-old girl with severe compression of the VA during rotation and extension of the head. (A) CT scan showing a supplementary piece of bone attached to the condyle (asterisk). (B) Angiography showing the VA preocclusive compression at the level of atlas (arrow). ((3) Operative view through bilateral posterolateral approach. Notice the course of the VAs (black stars) on the right side compared to the left side. O = occipital bone. C = occipital condyle. M = bony malformation. 2 = C2 nerve root.

COMPRESSION OF AND BY THE VERTEBRAL ARTERY 2 0 5

Fig 6. KlippeI-Feil malformation with fusion of Cl and C2. The contrast disappears on both sides during contralateral rotation. (A) Preoperative angiography on the left side with the head in neutral position (left) and rotated to the right side (right). Arrow indicates the level of compression. (B) Operative view through bilateral posterolateral approach. Only the right side is visible with the atlas (1) fused with the axis (2) and the VA (black star) with several loops. (C and D) Postoperative angiograms showing both VAs during contralateral rotation.

Fig 7. Bony malformation (supplementary condyle) com- pressing the VA and the neuraxis. (A) Preoperative CT scan. M = bony malformation. (B) Intraoperative view after the bony malformation has been drilled, working above and below the VA (black star) at Cl .

report of Husni et al, z 2 of 20 patients had unilateral compres- sion affecting a VA equal in size to the contralateral VA.

We studied 10 patients (unpublished data) who underwent VA angiography, for various problems. A dynamic study was per- formed with the head slightly extended and rotated between 60 ~ and 90 ~ We found only one patient with a significantly reduced VA diameter. Within the range of normal movements of the head and neck, the VA flow of some patients may be reduced signifi- cantly. Factors such as the depth of the groove of the atlas, hyper- trophy of the atlanto-occipital membrane, and excessive sliding of the altas in relation to the axis 5 may explain the occurrence of VA compression in only a few patients.

Patients with rotational obstruction might be at increased risk of complications after chiropractic manipulations. 34-3s In most reports of chiropractic accidents, the manipulations in- cluded extension and more or less forceful rotations. No bone fracture or luxation has been demonstrated. When performed, angiography has shown a dissecting hematoma stenosing or occluding the upper part of the VA. 38-42

Besides chiropractic manipulations, many activities cause VA compression, all of which share forced neck movements (mostly rotation): collision in contact sports, 43 archery, ~5 Ameri- can football, 44 swimming, 45 softball,36. 40 skiing, 46,47 hunting, 1 diving, 4s yoga exercises, 49 or ceiling painting.13

Therefore, any closed head or spine injury associated with neu-

rological symptoms, even transiently observed and without evi- dence of spinal fracture or luxation, should raise the suspicion of VA injury and lead to Doppler uhrasonographic studies, 3D-CT angiography, and/or angiography. In general, careful investigation of the circumstances of the injury reveals that the compression was caused by a forced movement combining rotation and extension. 2) Bow Hunter's Syndrome. Bow hunter's syndrome has been defined as symptomatic vertebrobasilar insufficiency due to mechanical stenosis or occlusion of a VA at C1-C2 when the head is rotated. 5,6,2~,5~ Surprisingly, most publications on this topic are Japanese. The name itself suggests the head position responsible for the VA compression. In some reports, no other factor than normal movements of the head has been found while different anomalies were identified in others. In the former re- ports, obstruction reflected the physiological rotational obstruc- tion as described above. In the latter, fibrous bands, 51 a thickened atlanto-occipital membrane, 5 or bony anomalies 52-53 were ob- served during surgery or on 3D-CT angiography. We suggest that these patients should not be classified the same as those whose etiology is only related to head position.

3D-CT angiography is the best examination for differentiat- ing patients with true Bow hunter's syndrome from the others. In Bow hunter's syndrome, this modality nicely shows the VA compression corresponding to a subluxation of the C1-C2 joint.6 s.33 In the other group, such a dislocation between C1 and C2 could not be demonstrated, and another factor was responsible for the VA compression.

The series by Matsuyama et al of 17 patients ~ includes 3 cases in which 3D-CT showed a dislodgement between C1 and C2 during rotation. Patients with very similar findings on 3D-CT have been reported by Morimoto et al. and by Kawaguchi et al. 7's

Hyperlaxity of the tendons and ligaments at the craniocervi- cal junction causing bilateral compression of the VA during head flexion-extension has been proposed to explain sudden death in newborns, ls,54 3) Other Causes of VA Compression at C1-C2. Besides Bow hunter's syndrome, several different factors have been reported at the origin of VA compression at C1-C2.

C2 Nerve Root

Surprisingly, the C2 nerve root can be too short and become stretched over the VA during contralateral rotation (Fig 4). One

Fig 8. Intraoperative view of a bone graft (asterisk) for fixa- tion after VA (black star) decompression. The bone graft is impacted between the occipital condyle and the C2 vertebral body.

COMPRESSION OF AND BY THE VERTEBRAL ARTERY 2 0 7

Fig g. Angiographic view of symptomatic VA compression by osteophytic spurs during contralateral rotation of the head at C3-C4 (arrow). Right side: head in neutral position. Left side: contralateral head position. Notice the minor compression at C5-C6 does not change during rotation (arrow heads).

such case was reported by Carney, and we observed a similar case. 23,s5 At surgery, the compression was obvious and varied during head movement; moreover, the VA expanded nicely as soon as the nerve was divided. Doubting that the C2 nerve root was the only factor, we obtained total control of the VA and opened the C1 and C2 transverse foramina without finding an associated compressive element.

ity at the craniocervical junction, severe injuries of the upper part of the spine are often associated with head injury. These cases are generally responsible for serious brain and spinal cord lesions leading to death or deleterious sequelae. Some nervous system lesions may be related to vertebrobasilar ischemia from VA injury. 43,44

4) Treatment (Fig 7 and 8). Despite controversies regarding treatment, fixation of the C1-C2 joint or a craniocervical fixa- tion seems reasonable when instability has been demonstrated, because instability threatens not only the VA but also the spinal cord. On the contrary, compressive elements that are not asso- ciated with instability do not require fixation. Decompression should follow the principles discussed previously, that is resec- tion of the compressing factor and opening of the adjacent (upper and lower) transverse foramina. This technique pro- vides excellent resolution of preoperative symptoms and does not limit head movement. Fixation is accomplished through a midline posterior approach, while decompression is generally achieved through an anterolateral approach. Some cases, for instance certain bone malformations, may require a combina- tion of decompression and fixation. If the malformation occurs on one side, either an anterolateral or a posterolateral approach can be used. If it occurs on both sides, a bilateral posterolateral approach is the best solution (see the article on surgical expo- sure in this issue).

V1 and V2 Segments

1) Osteophytes (Figs 9 and 10). Osteophytic spurs are the most common causes of a compression of the V2 seg- ment. ~,16,24,26,62-65 In some reports, the VA seemed to be dis- placed and exhibited a loop at the level of the osteophyte, but evidence of severe intermittent compression during a specific movement was lacking. Among many cases referred to us with suspicion of vertebrobasilar insufficiency from cervical spondy~

Bony Malformations (Fig 5 and 6)

Some bony malformations such as os odontoideum produce instability of the craniocervical junction with sliding of the head and atlas in relation to the axis. After this excessive move- ment, one or both VAs may be occluded. 52,~3,56-58 The mecha- nism is similar to that observed in other causes of atlantoaxial instability, such as fracture of the odontoid process 44,s9 and rheumatoid arthritis. 6~ Other bone malformations do not com- promise spinal stability but impinge upon the VA during head movement. The craniocervical junction is an elective site for various anomalies, 61 some of which may interfere with the VA, including supplementary condyle, Klippel-Feil syndrome, and anomaly of the C1-C2 joint. There are six such cases in our series, which we will discuss in the next issue. (See the article on Surgery around the Craniocervical Junction).

Trauma

Besides closed head and spine injuries, including forced head rotation without spinal fracture or luxation producing instabil-

Fig 10. MRI showing osteophytic VA compression. On the right side, the VA is not visible. The VAs are indicated by white asterisks.

2 0 8 GEORGE AND CARPENTIER

Fig 11. Abnormal level of entrance of the VA into the transverse canal on both sides at C4 (white asterisk) in the same patient.

tosis, we diagnosed intermittent VA compression caused by osteophytic spurs in only 5 cases. 23

When osteophytes occur on the unco-apophyseal joints, their most common site, the movement responsible for VA compression is head rotation. When they occur on facet joints, they are caused by extension of the neck. 66 Surprisingly, some published reports indicate either ipsilatera116,17,25,65,66 or con- tralateral 1,16,26,63 rotation as the movement that produces symptoms and VA compression. We found no publication in which 3D-CT angiography had been performed, and we have not observed a case recently enough to use this imaging study. Certainly, 3D-CT angiography should be of considerable help in understanding the mechanism of compression. In our five cases, the VA was always compressed during contralateral ro- tation.

Occasionally, permanent occlusion of the VA results from osteophytig compression. One such case, reported by Okuno et al.,4 resulted in spinal cord infarction. Repeated episodes of VA compression may produce intimal damage and blood stasis and eventually lead to thrombosis of the vessel, lo-13.67

As one may expect, the site of osteophytic compression is most often C4-C5 and C5-C6. Nagashima et al. 65 reported a distribution of 24% at C4-C5, 56% at C5-C6, and 20% at C6-C7.

Treatment must include unroofing the transverse processes proximal and distal to the level of compression and resection of the osteophytic spurs . 24,63-65 Partial treatment including only osteophytic resection may be successful but has been associated with failure. 8 Proximal and distal control of the VA is a safe policy before osteophytic resection; the osteophytes tend to adhere to the periosteal sheath of the VA, and their separation may be difficult. Frequently, this separation results in tears in the periosteal sheath and troublesome bleeding from the peri- vertebral venous plexus. VA exposure at some distance permits the venous bleeding to be easily controlled by bipolar coagula- tion, surgicel packing, or both. 2) Fibrous bands. Fibrous band is used as a general term to refer to fascial bands, tendons, muscles, or scar tis-

sue.2,25,51,68,69,7o Whatever the element, it involves a fixed struc- ture located anterior to the VA, which prevents the VA from moving anteriorly. During extension, the transverse process posterior to the VA displaces the VA anteriorly against the fibrous bands. The result is a cigar-cut effect on the VA. Often, this type of extrinsic compression is observed at the entrance of the VA into the transverse canal at C6 (Fig 11). The compress- ing effect is even more obvious if entrance of the VA into the transverse canal is at an abnormal level. 23,71 In this situation, the VA courses in front of the lower transverse process and has a bayonet-shaped course while traveling posteriorly to the up- per transverse process in which it enters (Fig 12). Whatever its level of entrance, the compression is located at the junction between a mobile and a fixed portion of the VA (Fig 13).

Most frequently, the compressive elements are the thickened tendons of the anterior scalenus muscle anterolaterally and of the longus colli muscle anteromedially. These 2 tendons are

Fig 12. Schematic drawing of VA compression by fibrous thickening of the tendons of the Iongus colli (L) and anterior scalenus muscles (S) attached to the transverse process (P). VA = black star.

COMPRESSION OF AND BY THE VERTEBRAL ARTERY 2 0 9

Fig 13. VA compression by fibrous bands at the artery's entrance into the transverse canal at C5. Angiographic view with the head (A) in the neutral position and (B) in extension.

attached on the transverse process. Some authors 64,69 believe that the thyrocervical trunk crossing the VA may contribute to VA compression, and they recommend dividing it and the mus- cle tendons. Hardin 64 and Dadsetan and Skerhut-Hei 72 believe that loops of the V1 segment may be associated with fibrous bands. To reduce the tortuosity of the VA, Hardin 64 suggests attaching the subclavian artery to the anterior scalenus muscle.

Notably, most so-called spontaneously dissecting hemato- mas are located at one of 2 sites: the C1-C2 segment or the C6 level where the VA enters the transverse canal and where most fibrous bands compressing the VA have been observed. This fact suggests that patients with a dissection at C6 may have

fibrous thickening of the muscle tendons offending the VA at this level.

Sell et al. reported a case in which extrinsic compression of the VA was associated with a thoracic outlet syndrome. The patient was a 44-year-old woman who complained of bilateral blindness during head rotation to the left. She also complained of paresthesia in the territory of the C7 and C8 nerve roots. Abduction of the arm was associated with a decreased radial pulse on the left side and with a. weakened hand grip. On angiography, the left VA was occluded 2 cm after the VA origin during rotation to the left. At surgery, the "lower cord of the brachial plexus" as well as the anterior scalenus tendon severely

2 1 0 GEORGE AND CARPENTIER

compressed the VA. After section of the anterior scalenus ten- don and resection of the first rib, all symptoms resolved.

The largest series of patients with fibrous bands ever reported was by Husni et al. 2 It included 20 patients: 12 men and 8 women ranging in age from 27 to 66 years (mean: 40 years). Intermit tent occlusion was unilateral in 15 patients and bi- lateral in 5 patients. In 18 patients the contralateral VA was hypoptastic. Of the 2 remaining cases, 1 patient presented with atherosclerotic stenosis at the origin of VA. There was no contralateral anomaly in the last case, and a mechanical obstruction at CI -C2 was suggested as the cause. All patients had only intermittent symptoms, normal neurological exam- inations, and no symptoms in the neutral head and neck position. At surgery, the compression was related to a thick tendon of the anterior scalenus muscle interdigitated with tendinous slips of the origin of the longus colli and scalenus medius muscles. In all case's the site of compression was just inferior to the C6 transverse process at the entrance of the VA into the transverse canal. Husni et al. r ecommend (1) resecting the lower segment of the anterior scalenus muscle, up to and including the tendon attached to the C6 transverse process, (2) dividing the longus colli tendon on the C6 transverse process, (3) obtaining absolute hemostasis, and (4) mobilizing a fat pad placed around the VA to avoid the development of fibrous scar tissue. 3) Other Factors of Intermittent Compression

Sympathetic Nerve

Two cases 23,74 of the sympathetic nerve compressing the first segment of the VA have been reported. Simply cutting the sympathetic element that crossed the anterior aspect of the VA a few millimeters after its origin released the compression and allowed symptoms to resolve. (See the article on Surgery of V1 and V2 in the next issue.)

Disc Herniation

In 1993 Budway et al. 3 reported a 45-year-old man who pre- sented with transient episodes of blindness, blurred vision, dizziness, and paraplegia. The neurological examination showed a right hemianopia and difficulty of heel-to-toe walking. Bilateral infarction of the occipital lobes was demonstrated on MR im- aging. On angiography, the left VA was completely occluded at C5-C6 and the size of the right VA was normal without anom- aly. Heparin treatment was begun, but after the patient pre- sented with anew episode of blindness, surgery was performed. The transverse foramina from C3 to C6 were opened. At C5, fragments of disc were discovered. Below this level, the VA was patent and pulsating while above no pulse could be detected. After the disc fragments were removed, the distal VA was re- opened as confirmed by intraoperative uhrasonography. Post- operatively, the patient suffered no further neurological symp- toms.

Tumors

Tumors occasionally induce intermittent VA compression. Typically, VA compression related to tumors is permanent and not associated with symptoms. The slow growth of tumors allows enough time for collateral pathways to develop suffi- ciently to compensate for reduced blood flow due to VA tom- pression even in the case of an occluded dominant VA 23,74 (Figs

Fig 14. Asymptomatic permanent occlusion of the VA at C3 (open arrow) by fibrous dysplasia. The small arrow indicates the anterior radiculomedullary artery. (Reproduced with per- mission from: The Vertebral Artery. Pathology and Surgery. B. George, C. Laurian. Springer-Verlag. Wien. New York. 1987. p 258).

14 and 15). The literature reports two cases in which VA tu- moral compression was symptomatic. In one patient, a neuri- noma at C3-C4 caused transient symptoms associated with head rotation to the left and concomittant occlusion of the right VA. 75 In another patient, an aneurysmal bone cyst 76 with ste- nosis of the VA was assumed to decrease further vertebrobasilar blood flow due to osseous compression of the dominant con- tralateral VA. However, this explanation was not supported by angiographic studies. In a third case, reported by Fields et a1.,77 VA stenosis caused by a C2 neurinoma was demonstrated by angiography, but simultaneous symptoms were not mentioned.

In our series of 114 cases of tumors associated with the VA, we observed only one intermittent compression due to an os- teochondroma at C2. The patient reported episodes of blurred vision and dizziness during head rotation. On presentation, however, symptoms had stopped, and angiography showed al- most complete occlusion of the left minor VA. The likely expla- nation is embolism from this small VA when it was almost completely occluded. We observed another patient who was aware of a huge supraclavicular mass for many years (Fig 16). The mass (an osteochondroma) grew slowly but was asymp- tomatic until the sudden onset of left hemianopia. On angiog- raphy, the right VA was occluded completely at its origin with severe displacement of the subclavian artery. Cerebral views

COMPRESSION OF AND BY THE VERTEBRAL ARTERY 2 1 1

Fig 15. Asymptomatic severe stenosis of the VA at C l caused by an extradural schwannoma. (A) Angiographic pre- operative view. (B) Intraoperative view through anterolateral approach. T = Tumor. P = Transverse process of atlas. 1 = VA at the C l level, 2 = VA at the C1-C2 level.

showed clear occlusion of the right posterior cerebral a r te ry- - highly suggestive of embolism.

In case of tumor, the VA is displaced first and then stenosed by being stretched over the transverse process. This process is well visualized at the entrance of the VA into the transverse canal (C6 transverse process) when tumors are present at the level of V1 (Fig 17).

Trauma

Fracture or .luxation of the spine is another cause of permanent VA compression. 26,44,7s-8~ Trauma is often responsible for VA injury but because angiography is rarely performed, it is seldom recognized. Willis et al. 78 reported 26 patients with trauma of the cervical spine, including subluxation with a facet lesion or a transverse foraminal fracture. A spinal cord injury was present in 13 patients. In 12 patients, angiography revealed a VA injury: 9 patients had occlusion and 3 patients had an intimal flap, dissecting hematoma, or pseudoaneurysm. Although spinal in- stability existed in all patients, in none of them did the VA injury clearly cause neurological dysfunction.

Another report by Louw et al. sl included 12 patients with either unilateral (5 cases) or bilateral (7 cases) facet joint dis- location. Five unilateral and one bilateral occlusions of the VA were observed but only two patients were symptomatic. In these reports by Willis et al. and Louw et al.,78,81 patients were selected who had spine lesions that could be expected to threaten the VA. In patients with spinal injuries, the incidence of VA injury is much lower. Parent et al. 9 saw only 5 cases of VA injury out of 640 patients with cervical spine fractures over 12 years. The most common finding in these 5 patients was a dislocation at C5-C6. As stressed by Parent et al., 9 an injury at V3 is generally the result of a minor neck trauma including rotation, while at V2 the mechanism tends to be more severe trauma associated with a shearing force or torsion.

Trauma also may be responsible for intermittent VA injury. It is often the result of spinal instability associated with a misdi- agnosed fracture or a pseudarthrosis. 59,s2

Treatment is first directed at immobilizing the spinal instability. Manipulation, which can worsen the patient's con- dition, must be avoided. 36 Anticoagulant therapy is recom- mended whenever dissection has been identified. Revascular- ization with venous bypass is rarely indicated in the acute phase. Persistent pseudoaneurysm may requ.ire venous bypass or endovascular treatment.

Compression by the Vertebral A r t e r y

The VA is sometimes the cause of neurovascular compromise. Because of a tortuous or anomalous course, the VA may contact cervical nerve roots or the spinal cord and cause radiculopa- thy s3-89 or myelopathy. 9~

Tortuosity

Tortuosity of the VA with loops often enlarges the interverte- bral foramen creating a radiographic appearance similar to hour-glass tumors. This tortuosity may occur at any level from C1-C291 to C5-C6. The most common site is C4-C5, followed by C3-C4 and C5-C6. 89 Both sides are affected equally. Bilateral loops are exceptional, however 83 (Fig 18).

We have seen one patient who was symptomatic with radic- ulopathy at C4-C5 and one with multiple bilateral loops from C3 to C6 who was asymptomatic. 7~ The only large series of symptomatic tortuosity was reported by Nishijima et al. 92 It included 44 patients, all of whom had kinking at the origin of the VA. Medical treatment failed to improve the patients' symp- toms. Surgery was performed on all patients to correct the kinking by rolling the subclavian artery forward and downward

212 GEORGE AND CARPENTIER

Fig 16. Huge osteochondroma extending from T2 to C4. (A) Standard radiograph (anteroposterior view) showing the calcified tumor. (B) Four-vessel angiography showing the displacement of the subclavian artery (arrow) and the occlusion of the right VA. (C) Cerebral angiography showing the occlusion of the right posterior cerebral artery with a defect in its lumen suggesting embolic clots (arrow).

COMPRESSION OF AND BY THE VERTEBRAL ARTERY 2 1 3

214 GEORGE AND CARPENTIER

Fig 18. Two examples of VA loops. (A) Unilateral loop at C4 (arrow). (B) Bilateral multiple loops from C3 to C6: left side angiography. On the right side bone erosion is visible along the vertebral bodies.

Fig 17. Severe tumoral compression of the VA at its entrance into the transverse canal. (A) CT scan and angiogram of a schwannoma (arrow heads). (B) Operative view through lateral approach with exposure of the VA (black star) compressed by the tumor (T) at the entrance of the transverse canal. P = Transverse process of C6. The internal jugular vein and carotid artery are retracted by the blade. Lateral to the tumor are located the cervical nerve roots (N). (C) Operative view after removal of the tumor. The VA (black star) is decompressed. Under the VA, the exit of the intervertebral foramen is visible. Notice the cervical nerve roots (N) and the sympathetic chain (S).

COMPRESSION OF AND BY THE VERTEBRAL ARTERY 2 1 5

consists of a VA in which one component pierces the dura at C1-C2 (Fig 19); the other component, which may be atretic, follows the normal course. (See the article on Surgical Anatomy in this issue). Few symptomatic cases in which segmental VAs compress neural elements have been reported. In every case, the VAs were in contact with the spinal cord, but only one 86 had symptoms of spinal cord compression with tetraparesis and sensory disturbances. In this case, however, cervical spinal ste- nosis was associated with the vascular anomaly. At surgery, both myelopathic factors were treated: the stenosis by laminec- tomy and the vascular compression by a Surgicel plug inter- posed between the spinal cord and the VA. The patient im- proved markedly after surgery. In other cases 9~176176 the accessory nerve (CN XI) was compressed. These cases were discovered after patients complained of torticollis. Surgical mi- crovascular decompression was associated with good out- comes.

Fig 19. Angiographic view of both VAs. On the right side, the course of the VA is normal. On the left side, the dura is penetrated by the VA at C2 and then has an intradural course rostral to the vertebrobasilar junction (small arrows). The asterisk indicates the normal location of the Cl -C2 segment of the VA. (Reproduced with permission from: The Vertebral Artery. Pathology and Surgery. B. George, C. Laurian. Springer- Verlag. Wien. New York. 1987. p 258).

by attachment of a branch artery to the clavicle. A satellite ganglionectomy was performed with this arterial fixation in every case.

Some characteristics of radiculopathy from vascular com- pression are lack of triggering factors, high frequency of pares- thesia of fingers, rarity of neurological deficit, and lack of noc- turnal recrudescence. 87

Anomalies of the VA

Anomalies in the VA course that cause neural compression are much less common than loops. A duplicate origin of the VA is an occasional anomaly, s6,93-99 The origin of the two trunks may be the subclavian artery, the brachiocephalic trunk, or the aor- tic arch. 1~176 The junction of the 2 trunks is most commonly at C5, but it has also been reported at C4 and C6. It may be associated with an internal carotid artery anomaly, a distal duplication of the VA, or a VA aneurysm.l~176 Only 1 case of compression of the sympathetic elements by a bifid VA has been reported. 1~176 The 70-year-old patient complained of occipital headaches and dizziness. The right VA had a duplicate origin with kinking of the 2 trunks, which joined at C4. The left VA ended at the PICA. At surgery, the satellite ganglion located between the 2 trunks was removed as well as the perivascular sympathetic and periarterial connective tissue. The patient's symptoms resolved completely over the next 3 years.

Duplication of the distal VA, also called the segmental VA,

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