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Microsurgical anatomy of the atlantal part of the vertebral artery
ELSEVIER
Anatomy
MICROSURGICAL ANATOMY OF THE ATLANTAL PART OF THE VERTEBRAL ARTERY Tarik H. Abd El-Bay, M.D.; Manuel Dujovny, M.D.; and James I. Ausman, M.D., Ph.D. Department of Neurosueery, University of Mnois at Chicago, Chicago, Illinois
Abd El-Bary TH, Dujovny M, Ausman JI. Microsurgical anatomy of the atlantal part of the vertebral artery. Surg Neurol1995;44:392401. BACKGROUND
Microanatomy of the vertebral artery has been the subject of multiple studies. However, none of them has covered every aspect of microvascular anatomy of the atlantal part of the vertebral artery. MATERIALS
AND
METHODS
Microsurgical anatomy of the atlantal part of the vertebral artery was studied in 14 cadaveric specimens. The artery was dissected using the standard microsurgical technique under operative microscope magnification. The atlantal part of the vertebral artery was divided into five segments:the foraminal, sagittal, transverse, medial condylar, and dural. The length of each segment was measured, as was the diameter of the artery. The branches of this part of the artery were identified and the distance between the point of dural entry of the artery and the midline of the atlantooccipital dura was measured. Distance between the mastoid tip and the artery and the distance between the mastoid tip and the tip of Cl transverse process were measured. RESULTS
Results of all measurements are summarized in tables and text. We discuss various anomalies, branches, and lesions of the vertebral artery and surgical approaches with new methods of managing diseasesin this area. KEY WORDS
Atlantai, microanatomy, vertebral artery.
T
he object of this study was to detail the microvascular anatomy of the atlantal part of the vertebral artery (VA). Although this section of the artery has been studied before, to our knowledge none of these studies covered the atlantal part in every aspect [9,15,16,25,28]. Being deeply buried at the craniocervical junction, an area where large varieties of lesions are found, a thorough study of Address reprint requests to: Manuel Dujovny, M.D., Neuropsychiatric Institute, The University of Illinois at Chicago, Department of Neurosurgery (M/C 799). 912 South Wood Street, Chicago, IL 60612-7329. Received December 17, 1993; accepted January 1, 1995. 00903019/95/$15.00 SSDI 0090-3019(95)00035Z
its anatomic structures may make surgical interventions less complicated. The vertebral artery is traditionally divided into four segments. In the first segment, the artery angles dorsally from its origin at the subclavian artery until it enters the transverse foramen of the C6. The second segment lies within the transverse foramen from C6 to C2. The third portion is the distal extracranial segment that is short and tortuous. The artery passes through the transverse foramen of the atlas and then bends abruptly around the superior articular process of the atlas. It then makes a sharp turn to pierce the dura mater, thereby entering the cranium through the foramen magnum. The fourth segment is entirely intracranial and terminates when the vertebral arteries join at the medullopontine junction to form the basilar artery [4,16].
MATERIALANDMETHODS This study was performed on 14 cadaveric specimens having no history of craniocervical pathology. The ages of the specimens were not defined. Vertebral artery measurements and anatomic relationships were studied under an operative microscope (OPMI I-SH: Carl Zeiss Inc., New York, NY) with a video camera recording (Hitachi Denshi, Ltd., Japan). Dissection was made using microsurgical instruments. The atlantal part of the third portion of
the VA was divided (Figure 1):
into five segments,
as follows
Foraminal segment: From point of entry to Cl transverse foramen to the point of direction change from vertical to posterior in the sagittal plane. SagittaI segment: From the end of the first segment to the change of direction from the sagittal to the transverse in the horizontal plane above the Cl posterior arch. 655 Avenue
0 1995 by Elsevier Science Inc. of the Americas, New York, NY 10010
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0
Vertebral Artery (Atlantal Part) (mm) SEGMENT
-Fs
Drawing of atlantal part of vertebral artery (VA) showing different segments: foraminal (Fs), sagittal (Ss), transverse (I?.), medial condylar @KS), and dural (Ds). The dura mater is opened posteriorly and the intradural vertebral artery is shown to go anterior to the brain stem (from Lang [17] with modification, 41).
0
Transverse segment: Starting from the end of the second segment and running an arched course above the Cl posterior arch with part of its course in the transverse groove of atlas vertebra to the direction change from transverse to vertical medially to the lateral mass of the atlas. Medial condylar segment: From the end of the third segment and running superomedially to the atlanto-occipital joint and occipital condyle, entering the dura at the lateral margin of the foramen magnum. Dural segment: The part of the artery surrounded by dural sheath. The specimens were positioned supine with a 30-degree head tilt to the other side during skin incision and muscle dissection. The head tilt was increased up to 75 degrees while dissecting the artery and taking the measurements. We removed part of the posterior arch of Cl and unroofed the Cl transverse foramen to facilitate taking measurements. The branches of this part of the artery were studied, and the relations to the Cl nerve, vertebral venous plexus, and the mastoid process were identified. MEASUREMENTS The length of each segment was measured except for the third segment; because of its curved course, the distance between the end of the sagittal segment and the beginning of the fourth segment was measured instead. In the dural segment the length of the dural sheath medial and lateral to the artery
393
Foraminal Sagittal Transverse Medial condylar Dural Medial side Lateral side
LEFT MEAN RANGE 10
RIGHT MEAN RANGE
8-13
10.1
8.5
6-13
8.9
16.6 9.8
13-20 8-12
16.1
8-14 6-l 13-19
8.8
6-14
5 3
46 2-5
4.4 2.7
2-6 1.5-4
was measured (Table 1). The diameter of the artery was measured at three positions: at the point of entry to the Cl transverse foramen; at the transverse groove of Cl; and at its dural entry. Five other distances were measured: the distance between the point of dural entry and the midline of the atlantooccipital dura; the distance between the point of direction change of the artery from sagittal to transverse above the Cl transverse foramen and the mastoid tip; the distance between the tip of the Cl transverse process and the mastoid tip; the distance between the point of origin of the posterior meningeal artery and the point of dural entry of the VA, and the distance between the point of origin of the muscular branch above Cl and the point of direction change from sagittal to transverse above the Cl transverse foramen.
RESULTS VERTEBRALARTERY The VA entered the transverse foramen of Cl where it ran in a vertical and slightly anterior direction. Just above the Cl transverse foramen, the artery changed direction dorsally and ran farther in the sagittal plane. In most cases this change of direction was associated with an acute angle, but in others it was in a posteromedial direction. Then the artery changed direction again and ran transversely above the posterior arch of Cl. The distance between the mastoid tip and the point of direction change of the artery from sagittal to horizontal was 2 1 mm (mean) on the left side (12-30-mm range) and 21.2 mm (mean) on the right side (12-30-mm range) (Figure 2). This part of the artery ran a straight or arched course depending on the length and direction of the second segment of the artery. If the length of the second part was long the artery ran in a straight course, and if it was short the artery ran in an arched course with posterior protrusion above the Cl posterior arch. This posterior
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of atlantal part of qtweenVADrawing showing: distance bemastoid tip and VA; mastoid tip and tip of Cl transverse process; distance between point of dural entry and midline of atlanto-occipital dura (from Lang with modification, 39).
protrusion of the artery was 11 mm in one specimen. In this situation the artery could be injured during some operations at the craniocervlcal junction. This part of the artery related anteriorly to the lateral mass of the atlas and atlanto-occipital joint. It passed in the transverse groove above the Cl posterior arch to the point of direction change from transverse to vertical at the medial side of the lateral mass of the atlas and occipital condyle. The direction change usually occurred at the end of the transverse groove medially but in one specimen it changed its direction in the middle of the groove. The artery then passed upward and medially, partially covered by the atlanto-occipital membrane, and entered the dura at the lateral aspect of the foramen magnum. At that part of the artery, the dura formed a funnel-shaped sheath around the artery. The length of this sheath was longer medial to the artery than lateral to it. The distance between the point of dural entry and the midline of the atlantooccipital dura was 16.8 mm (lo-19.5-mm range) (Figure 2). The diameter of the artery was found to be 4 mm on the left side (2.5~6-mm range) and 3.9 mm on the right (2.3-5.5-mm range); there was no change of the artery diameter in its atlantal part (Table 2). The Cl transverse process has an important role in the approach to this part of the VA. It is the most prominent transverse process of the cervical spine and can be palpated subcutaneously halfway between the mastoid tip and the angle of the mandible. The distance between the tip of the Cl transverse process and the mastoid tip was measured. On the left side it was 21 mm (15-30-mm range), on the right side, 18.8 mm (1 l-25-mm range) (Figure 2).
BRANCHES As the artery entered the transverse foramen of Cl, it formed a radiculomuscular branch below the Cl posterior arch that ran medially to the atlantoaxial joint anteriorly and C2 nerve inferiorly. This branch was found in all specimens. It divided into a dural branch that entered the dura with the C2 nerve and muscular branches. This radiculomuscular branch originated just at the point of entry of the VA to the Cl transverse foramen, but in one case it originated at the lower part of the foramen (Figure 3). Above the Cl posterior arch the artery formed another muscular branch directed posterosuperiorly and medially. This branch was found in four specimens. The point of origin of this artery was 5-10 mm distal to the point of the VA direction change from sagittal to transverse above the Cl posterior arch (junction between sagittal and transverse segments) (Figures 3 and 4). Distal to this branch the VA projected another branch from the posteromedial aspect, the posterior meningeal artery. It traversed a tortuous course to enter the dura. The point of origin of this artery was 7-l 1 mm proximal to the point of dural
q
Diameter of Vertebral Ariery (mm) SIDE
Left Right Left greater than right Right greater than left Left equal to right
MEAN 4
3.9
’ RANGE 2.5-6 2.3-5.5
42.9% 35.7%
21.4%
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(A): Atlanta1 part of VA showing C2 nerve going 1 (A): Sagittal and transverse of atlantal part of VA. q(RMbr)around Cl-C2 part of VA. Radiculomuscular branch 0 Muscular branch (Mbr), periosteal sheath (PSh), at entry to Cl transverse foramen, muscular venous plexus (VP), and Cl posterior arch. (3): Drawing
branch (Mbr) from transverse part, occipital condyle (OcC), Cl (Cl) posterior arch, transverse process (‘fP>, and atlanto-occipital membrane (AOcM). Cl transverse foramen is opened posteriorly and part of the posterior arch of atlas is removed. (B): Drawing of previous figure.
entry of VA. This artery was found on the left side in
four specimens, on the right in six, and absent in four. The posterior spinal artery originated at the posteromedial part of the artery at the point of the dural entry. It was found on the left side in four specimens, and on the right in five (Table 3). VERTEBRAL VENOUS PLEXUS The VA was surrounded by a plexus of veins, continuous with the condylar emissary vein above and with veins below the Cl posterior arch around the C2 nerve and the radicular branch of the VA below. This plexus
drained
into two venous
channels
that
accompanied ramen of Cl. or posterior the foramen
the artery through the transverse foThese two veins were lateral, medial, but never anterior to the artery inside (Figure 5).
of previous figure.
PERIOSTEAL SHEATH The artery and part of the venous plexus were surrounded by a periosteal sheath that encircled the whole course of the artery up to the point of dural entry, where it adhered to the dura mater. This sheath was calcified, converting the transverse groove into a complete tunnel in three specimens, and into a partial tunnel in four specimens (Figure 6).
q
Branches of the Atlanta1 Part of Vertebral Artery NUMBER BRANCH
Radicufomuscular Muscular Postmeningeal Postspinal
PERCENTAGE
LEFT
RIGHT
LEFT
RIGHT
14 4 4 4
14 4 z*
100 28.6 28.6 28.6
100 28.6 42 35.7
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(A): Transverse segment of atlantal part of VA after opening periosteal sheath (PSh) showing venous plexus (VP) surrounding the artery (VA), and Cl posterior arch (Cl). (B): Drawing of previous figure.
Cl
NERVE
The Cl nerve exited the dura medial to the artery through the funnel-shaped dural opening. It continued downward and laterally to run inferior and slightly anterior to the artery in the transverse groove. At the transverse groove the nerve branched around the artery to supply the muscles of the posterior triangle of the neck. As the VA enters the Cl transverse foramen the nerve continued anteriorly to the artery and divided into muscular branches (Figure 7).
(A): Transverse of atlantal part of VA, showing calq(Cal.m PSh). cification of periosteal sheath around the artery (B): Drawing of previous figure.
DISCUSSION Within the long history of vascular surgery, the vertebral artery has a small place due to its deep location and difficult access for exploration. Sanson (1836) stated that the VA is beyond the reach of surgery. Since that date many surgeons have suc-
ceeded in operating on the VA, starting with Maisonneuve (1853) who first successfully ligated the first portion of the vertebral artery. Later Fenger (1881) performed a successful ligation on the third
Microsurgical
Anatomy of the Vertebral Artery
B (A): Atlanta1 part of VA after removal of foraminaf, sagittal, and half the transverse segment, showing Cl nerve (Cln) as it goes anteroinferior to artery and continues laterally to supply muscles in this area. It also shows condylar vein (CV), Cl posterior arch (Cl), Cl transverse foramen (TP), Cl transverse process, venous plexus (VP) and occipital condyle (OcC). (B): Drawing of previous figure.
part of the artery when he treated a traumatic aneurysm in a 19-year-old man [ 111. In 1888 Matas described the first operation on an aneurysm of the distal part of the artery using a posterior approach [22]. Following this, ligation of the artery was proposed in different cases with various indications: epilepsy (2) brain tumors (7) and arteriovenous fistulas (8). A major advance in the diagnosis of VA diseases was made after the introduction of angiography [23]. Nevertheless, until the end of the 1950s surgery of the VA remained directed to arteriovenous fistulas and aneurysms of traumatic origin. In 1959 Cate and Scott performed the first endarterectomy of the proximal VA [6]. Following the development of vascular surgery, a better understanding of the role of the VA in cerebral ischemia, and improvement in surgical techniques, preservation
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and revascularization of the VA contributed to more effective surgical intervention in this region. Artery diameter in our specimens was 4 mm on the left side and 3.9 mm on the right. Francke and coworkers found arterial diameters of 4.7 mm on the left side and 4.3 mm on the right [9]. The vertebral arteries are frequently asymmetric. Sometimes the minor VA is too small to be detected by angiography, and it may end in the posterior inferior cerebellar artery. If this minor VA ends in the basilar trunk it is termed hypoplastic; if it is not connected to the basilar artery it is termed atretic. Sometimes the artery may be completely absent. In that case it is frequently replaced by persistent congenital anastomoses [35]. There are four possible persistent congenital anastomotic arteries, and three of them are intracranial: the trigeminal, otic, and hypoglossal. One, the proatlantal, is extracranial. They represent persistent embryonic anastomotic arteries between the carotid and basilar circulatory systems. The proatlantal is a rudimentary channel that forms the proximal portion of the occipital artery. The occipital artery originates from the internal carotid and connects later with the external carotid artery. This explains why two types of proatlantal arteries may be observed, one arising from the external carotid and the other from the internal carotid. In both types, the artery forms a sharp curve after its origin to rest upon the supe rior aspect of the transverse process of Cl. It does not pass through the transverse foramen of any vertebra before entering the skull through the foramen magnum, since it joins the normal course of the VA. In case of a persistent proatlantal artery, the vertebral artery is absent or hypoplastic. This suggests that the proatlantal artery persists because of the failure of normal vertebral artery development [ 18,19,27,29,34,35]. Another anomaly of the VA is duplication or fenestration of the artery. This is extremely rare in persons of Western European descent, but in Japanese people it is present in 1% of patients. It occurs predominantly in the upper cervical region and is associated with other intracranial anomalies. It occurs when a primitive segmental artery persists during the embryologic development of the artery. With duplication, either the main trunk penetrates the dura at the Cl-C2 levels and the atretic or hypoplastic trunk follows the normal course, or there are two trunks of equal size, one extradural and the other intradural. This may cause an acute subdural hematoma and death, following lateral cervical spine puncture [30,36,37]. Calcification of the periosteal sheath around the artery is a common finding. Oliveria and colleagues
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reported that 28% of their cases had a complete canal, 24% had a partial canal, and 48% had a shallow groove [25]. Lamberty and Zivanovic reported in their series that 15% had a complete canal, 22% had a partial canal, and 63% had a shallow groove [ 151. Radojevic and Negovanovic found a bony canal bilaterally in 7% of cases, unilaterally in 14%, and an incomplete bony canal in 2% of their specimens [28]. To avoid kinking and subsequent possible brain stem infarction, calcification of the periosteal sheath and tunneling of the transverse groove should be considered during operations requiring mobilization of the artery, especially if the artery is the dominant one. In our study the posterior meningeal artery was found on the left side in four specimens, on the right side in six. The meningeal branches of the VA are usually small, but may become significantly enlarged in a variety of pathologic conditions. Both anterior and posterior meningeal branches arise from the extracranial VA and supply a portion of the dura of the posterior fossa. Newton reported the posterior meningeal artery on the right side in 29.8% of their cases and on the left side in 40% (angiographic study) [24]. This artery originates from the posterior portion of the VA between the arch of the atlas and the base of the skull. The artery courses backwards and upwards toward the posterior rim of the foramen magnum. Its course is slightly tortuous in its proximal extracranial portion. After entering the skull it assumes a straighter course extending superiorly, parallel, and close to the inner table of the occipital bone. It could occasionally be followed to the internal occipital protuberance and, rarely, could be seen extending more superiorly up to the level of the tentorium [24]. We found the posterior spinal artery on the left side in four specimens, and on the right in five. It usually arose from the posteromedial surface of the VA at the point of its dural entry or from the intradural part of the artery [5,25]. In the subarachnoid space, the artery coursed medially behind the most rostra1 attachments of the dentate ligament, and upon reaching the lower medulla it divided into ascending and descending branches. The ascending branch coursed through the foramen magnum and supplied the restiform body, the gracil and the cuneate tubercles, the rootlets of the accessory nerve, and the choroid plexus near the foramen of Magendie, and may have given off branches which anastomosed with branches of the posterior inferior cerebellar artery. The descending branch passed downward on the posterolateral surface of the spinal cord between the dorsal rootlets and the dentate ligament. It anastomosed with the posterior
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branches of the radicular arteries that entered the vertebral foramen at lower levels. The descending branch gave off collateral branches, each lower one being smaller and less constant than the previous one. They coursed medially across the posterior surface of the spinal cord and joined to form an artery located in the midline, parallel to the posterior spinal arteries [25]. The posterior inferior cerebellar artery (PICA) is the largest branch of the vertebral artery; it has a variable site of origin from the foramen magnum to the vertebrobasilar junction. Akar et al found the artery to originate 16.4 mm (3.0-25.0 mm) from the vertebrobasilar junction; none of the PICA originated below the foramen magnum in their study [ 11. However, Lister et al reported the origin of the PICA below the foramen magnum in 7 out of 42 PICAS, and the origin was located 16.9 mm from the vertebro-basilar junction (o-35.0 mm range) [20]. Margolis and Newton [21] found the origin of the PICA between 24 mm below and 45 mm above the foramen magnum. In their study, 18% of PICAS originated below the level of the foramen magnum, 4% at the level, and 57% above the level of the foramen magnum; the site of origin was 16.0 mm (O-35.0-mm range) from the vertebrobasilar junction. The PICA was noted to present as a single artery in 90% of cases, duplicated in 6%, and absent in 4%. In case of absent PICA, the anterior inferior cerebellar artery branches supply the territory of the PICA. Lister et al divided the PICA into five segments: the anterior medullary segment in front of the medulla; the lateral medullary segment, which courses beside the medulla and extends to the origin of the glossopharyngeal, vagal, and accessory nerves; the tonsillomedullary segment, which courses around the caudal half of the cerebellar tonsil; the telovelotonsilar segment, which courses in the cleft between the tela choroidea and the inferior medullary velum rostrally and the superior pole of the cerebellar tonsil caudally; and the cortical segment, which runs over the cerebellar surface [20]. The Cl nerve was found in all cases to exit the dura medially to the artery, moving anteromedially to the artery down to the transverse groove, then inferiorly and slightly anteriorly to the artery in the transverse groove of Cl. It continued anteriorly to the artery as it entered the transverse foramen of Cl. The Cl nerve was formed mainly of anterior root. The posterior root was inconstant and was variably found to be intimately related to the presence or absence of connection with the spinal nerve. Ouaknine and Nathan reported the absence of Cl posterior root in 64% of their specimens [26].
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There are various possibilities of nerve supply in areas normally innervated by the Cl posterior root, as well as the central course of the sensory fibers of Cl. These possibilities include a normal course through the Cl posterior root and connection with the accessory nerve via anastomosis. The central fibers still reach the medulla and spinal cord, passing directly into the posterior root, although it is possible that some fibers reach the medulla with the accessory nerve. Other possibilities are that sensory fibers reach the medulla through the rootlets of the 11th cranial nerve (almost half of all specimens), and the rest take over the corresponding area of Cl by C2 rootlets that will reach the spinal cord by the same nerve root or by the 11th cranial nerve. The Cl posterior root participates in the innervation of the meninges, the atlanto-occipital joints, and the area of the occipital for-amen [26]. The neurosurgical significance of Cl posterior rootlets becomes apparent in neurotomy operations. Including these rootlets in radiculotomy will avoid residual pain after sectioning C2 and C3 dorsal roots in cases of lesions causing intractable pain at the craniocervical junction [26]. The atlantal part of the VA can be approached by different routes: lateroanterior, dorsolateral [ 131, and posterior [3]. The lateroanterior approach is recommended by many authors [ 10,12,14,32,33, 38,39,40]. It provides relatively easy access to any part of the VA, from its ostium up to the intracranial portion, which is wide and safe. This approach passes through the anatomic plane between the sternocleidomastoid muscle and the internal jugular vein without any vessel to dissect. The only element crossing the field in this approach is the accessory spinal nerve that has to be freed. In addition, numerous other structures can be controlled by the lateroanterior approach including the carotid artery, cervical nerve roots, hourglass tumors, and vertebral bodies. Hemilaminectomy of Cl and C2, hemicraniectomy, and infratemporal ap proaches follow the same technique as the lateroanterior approach [ 111. The importance of controlling the VA without opening the periosteal sheath must be stressed to avoid problems with the perivertebral venous plexus. Moreover, with periosteal dissection the VA is protected surgically. There are two sites that need particular attention. The first is the curvature of the VA when it leaves the groove of the atlas to join the dura mater. There are two identifying landmarks of this site: change in height of the posterior aspect of the atlas, which increases just medially to this point, and a muscular branch (the suboccipital artery), which originates at this point. The second site is the dural penetra-
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tion of the VA. It is not advisable to free the artery completely at this level, since the periosteal sheath is particularly adherent to the dura mater. It is safer to cut the dura mater around but at some distance from the VA [ 121. The muscular branch above the posterior arch of the atlas is usually harvested during exposure of the artery, and care must be taken not to confuse the VA with the posterior inferior cerebellar artery that may rarely originate from the extradural VA [16,17,20,31,41]. REFERENCES 1. Akar ZC, Dujovny M, Slavin KV, Gomez-Tortosa E, Ausman JI. Microsurgical anatomy of the intracranial part of the vertebral artery. Neurol Res 1994;16:17180. 2. Alexander W. The treatment of epilepsy by ligature of the vertebral arteries. Brain 1882;5:170-87. 3. Ausman JI, Diaz FG, Pearce JE, de 10s Reyes RA, Leuchter W, Mehta B, Pate1 S. Endarterectomy of the vertebral artery from C2 to posterior inferior cerebellar artery intracranially. Surg Neurol 1982;18:400-4. 4. Caplan LR. Vertebrobasilar system syndromes. In: Vinken PJ, Bruyn GW, Klawans, eds. Handbook of clinical neurology. Vascular disease. Part 1. Amsterdam: Elsevier Science Publisher B.V, 1988;53:371-409. 5. Carpenter MB. Neuroanatomy. 4th ed. Philadelphia: Williams and Wilkins, 1991:449. 6. Cate WR, Scott HN. Cerebral ischaemia of central origin: relief by subclavian vertebral artery thromboendarterectomy. Surgery 1959;45:19-31. 7. Dandy WE. Intracranial arterial aneurysm. Ithaca: Comstock Publishing Co., 1944. 8. Elkin DC, Harris MH. Arteriovenous aneurysm of the vertebral vessels: report of ten cases. Ann Surg 1946; 124:934-51. 9. Francke JP, Diemarino V, Pannier M, Argenson C, Libersa C. The vertebral arteries. The V3 atlanto-axial and V4 intracranial segments collaterals. Anat Clin 1981;2:229-42. 10. George B, Laurian C. Surgical approach to the whole length of the vertebral artery with special reference to the third portion. Acta Neurochir (Wien) 1980;51: 259-72. 11. George B, Laurian C. The vertebral artery. In: Pathology and surgery. New York: Springer-Verlag, 1987;117:146-50. 12. George B, Dematons C, Comphignon J. Lateral approach to the anterior portion of the foramen magnum: application to surgical removal of 14 benign tumours: technical note. Surg Neurol 1988;29:484-90. 13. Gilsbach JM, Eggert HR, Seeger W. The dorsolateral approach in ventrolateral craniospinal lesions. In: Textbook of diseases in the crania-cervical junction. New York: Walter de Gruvter, 1987:369-73. 14. Jonson RM, Murphy MJ, Southwick WO. Surgical approach to the spine. In: Rothman RH, Simeone FA, eds. The spine. Philadelphia: W.P. Saunders Co, 1992: 1607-33. 15. Lamberty BGH, Zivanovic S. The retro-articular vertebral artery ring of the atlas and its significance. Acta Anat 1963;85:113-22.
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37.
38. 39. 40. 41
basilar anastomosis. Am J Roentgen01 Radiat Ther Nucl Med 1975;124:281-6. Tokuda K, Miyasaka K, Abe H, Takei H, Sugimoto S, Tsuru M. Anomalous atlantoaxial portions of verte bra1 and posterior inferior cerebellar arteries. Neuroradiology 1985;27:410-3. Vincentelli F, Giuseppe C, Rabehanta PB, Rey M. Surgical treatment of a rare congenital anomaly of the vertebral artery: case report and review of the Iiterature. Neurosurgery 1991;28:416-20. Watkins RG. Surgical approaches to the spine. New York: Springer-Verlag, 1983:1-25. Whitesides TE, Kelly RP. Lateral approach to the up per cervical spine for anterior fusion. South Med J 1966;59:879-83. Whitesides TE. Lateral retropharyngeal approach to the upper cervical spine. In: The cervical spine. 2nd ed. Philadelphia: JB Lippincott Co, 1989:796-804. Yasargil MG. Microneurosurgery. New York: George Thieme-Verlag, 1984; 1:130.
COMMENTARY This article by T. H. Abd El-Bar-y and associates is an important adjunct to our knowledge of the anatomy of the craniocervical junction area. It provides many precise details and measurements about the relationships of the vertebral artery and the neighboring structures. The upper cervical vertebral artery is a key which provides many possibilities for approaching several different areas: the upper cervical spine, the foramen magnum, and the foramen jugulare. Being able to expose and control the vertebral artery permits one to treat lesions directly involving this vessel, such as tumors (osseous tumors, sarcomas, extradural Cl or C2 neurinomas, extradural meningiomas), craniocervical junction malformations, or infectious processes. In these lesions, generally the entire length of the third vertebral artery segment between C2 and the dura has to be exposed, and sometimes transposed. Vertebral artery control improves or provides access to intradural lesions of the foramen magnum to the odontoid
and anterior
arch of the atlas, and to the
foramen jugulare. Obviously, it also allows one to suppress the vascular supply of tumors such as paragangliomas, or to treat arteriovenous fistulae, though endovascular
techniques
most often make it
useless. Finally, the Cl-C2 segment of the vertebral artery is the site of choice for distal revascularization in case of proximal flow compromise (ostial occlusion) or risk of embolism from vascular lesions (aneurysm) and endovascular treatments. All these surgical techniques are quite reliable, providing adequate exposure of the vertebral artery is achieved [ 1,2,3 1. One very important point stressed by the authors is the periosteal sheath surrounding
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the vertebral artery and the venous plexus. In all cases, the vertebral artery must first be controlled out of this periosteal sheath to avoid any troublesome bleeding from the venous plexus. If the vessel wall has to be controlled (for instance, to perform a venous bypass), the sheath is opened in a second step. The control of the vertebral artery requires perfect knowledge of the anatomy of this vessel, with all possible variations and anomalies. Dr. Abd El-Bary and his colleagues must therefore be thanked for the anatomic details given in their article, of which any surgeon
working in the region of the craniocervical tion should be aware. Bernard
VERY GUN THAT IS FIRED, EVERY WARSHIP LAUNCHED, EVERY ROCKET FIRED, SIGNIFIES, IN THE FINAL SENSE, A THEFT FROM THOSE WHO HUNGER AND ARE NOT FED, THOSE WHO ARE COLD AND ARE NOT CLOTHED. THE WORLD IN ARMS IS NOT SPENDING MONEY ALONE. IT IS SPENDING THE SWEAT OF ITS LABOURERS, THE GENIUS OF ITS SCIENTISTS, THE HOPES OF ITS CHILDREN. GENERAL,
junc-
George, M.D. Paris, France
REFERENCES 1. George B, Laurian C. The vertebral artery: pathology and surgery. New York: Springer Verlag, 1987. 2. George B, Lot G, Velut S. Tumors of the foramen magnum. Neuorchirurgie 1993;39:1-92. 3. George B, Laurian C. Impairment of vertebral artery flow caused by extrinsic lesions. Neurosurgery 1989; 24:206-14.
E
U.S.
401
DWIGHT D. EISENHOWER (1890-l 969) REPUBLICAN POLITICAN, PRESIDENT SPEECH, APRIL 1953
Anatomy
MICROSURGICAL ANATOMY OF THE ATLANTAL PART OF THE VERTEBRAL ARTERY Tarik H. Abd El-Bay, M.D.; Manuel Dujovny, M.D.; and James I. Ausman, M.D., Ph.D. Department of Neurosueery, University of Mnois at Chicago, Chicago, Illinois
Abd El-Bary TH, Dujovny M, Ausman JI. Microsurgical anatomy of the atlantal part of the vertebral artery. Surg Neurol1995;44:392401. BACKGROUND
Microanatomy of the vertebral artery has been the subject of multiple studies. However, none of them has covered every aspect of microvascular anatomy of the atlantal part of the vertebral artery. MATERIALS
AND
METHODS
Microsurgical anatomy of the atlantal part of the vertebral artery was studied in 14 cadaveric specimens. The artery was dissected using the standard microsurgical technique under operative microscope magnification. The atlantal part of the vertebral artery was divided into five segments:the foraminal, sagittal, transverse, medial condylar, and dural. The length of each segment was measured, as was the diameter of the artery. The branches of this part of the artery were identified and the distance between the point of dural entry of the artery and the midline of the atlantooccipital dura was measured. Distance between the mastoid tip and the artery and the distance between the mastoid tip and the tip of Cl transverse process were measured. RESULTS
Results of all measurements are summarized in tables and text. We discuss various anomalies, branches, and lesions of the vertebral artery and surgical approaches with new methods of managing diseasesin this area. KEY WORDS
Atlantai, microanatomy, vertebral artery.
T
he object of this study was to detail the microvascular anatomy of the atlantal part of the vertebral artery (VA). Although this section of the artery has been studied before, to our knowledge none of these studies covered the atlantal part in every aspect [9,15,16,25,28]. Being deeply buried at the craniocervical junction, an area where large varieties of lesions are found, a thorough study of Address reprint requests to: Manuel Dujovny, M.D., Neuropsychiatric Institute, The University of Illinois at Chicago, Department of Neurosurgery (M/C 799). 912 South Wood Street, Chicago, IL 60612-7329. Received December 17, 1993; accepted January 1, 1995. 00903019/95/$15.00 SSDI 0090-3019(95)00035Z
its anatomic structures may make surgical interventions less complicated. The vertebral artery is traditionally divided into four segments. In the first segment, the artery angles dorsally from its origin at the subclavian artery until it enters the transverse foramen of the C6. The second segment lies within the transverse foramen from C6 to C2. The third portion is the distal extracranial segment that is short and tortuous. The artery passes through the transverse foramen of the atlas and then bends abruptly around the superior articular process of the atlas. It then makes a sharp turn to pierce the dura mater, thereby entering the cranium through the foramen magnum. The fourth segment is entirely intracranial and terminates when the vertebral arteries join at the medullopontine junction to form the basilar artery [4,16].
MATERIALANDMETHODS This study was performed on 14 cadaveric specimens having no history of craniocervical pathology. The ages of the specimens were not defined. Vertebral artery measurements and anatomic relationships were studied under an operative microscope (OPMI I-SH: Carl Zeiss Inc., New York, NY) with a video camera recording (Hitachi Denshi, Ltd., Japan). Dissection was made using microsurgical instruments. The atlantal part of the third portion of
the VA was divided (Figure 1):
into five segments,
as follows
Foraminal segment: From point of entry to Cl transverse foramen to the point of direction change from vertical to posterior in the sagittal plane. SagittaI segment: From the end of the first segment to the change of direction from the sagittal to the transverse in the horizontal plane above the Cl posterior arch. 655 Avenue
0 1995 by Elsevier Science Inc. of the Americas, New York, NY 10010
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0
Vertebral Artery (Atlantal Part) (mm) SEGMENT
-Fs
Drawing of atlantal part of vertebral artery (VA) showing different segments: foraminal (Fs), sagittal (Ss), transverse (I?.), medial condylar @KS), and dural (Ds). The dura mater is opened posteriorly and the intradural vertebral artery is shown to go anterior to the brain stem (from Lang [17] with modification, 41).
0
Transverse segment: Starting from the end of the second segment and running an arched course above the Cl posterior arch with part of its course in the transverse groove of atlas vertebra to the direction change from transverse to vertical medially to the lateral mass of the atlas. Medial condylar segment: From the end of the third segment and running superomedially to the atlanto-occipital joint and occipital condyle, entering the dura at the lateral margin of the foramen magnum. Dural segment: The part of the artery surrounded by dural sheath. The specimens were positioned supine with a 30-degree head tilt to the other side during skin incision and muscle dissection. The head tilt was increased up to 75 degrees while dissecting the artery and taking the measurements. We removed part of the posterior arch of Cl and unroofed the Cl transverse foramen to facilitate taking measurements. The branches of this part of the artery were studied, and the relations to the Cl nerve, vertebral venous plexus, and the mastoid process were identified. MEASUREMENTS The length of each segment was measured except for the third segment; because of its curved course, the distance between the end of the sagittal segment and the beginning of the fourth segment was measured instead. In the dural segment the length of the dural sheath medial and lateral to the artery
393
Foraminal Sagittal Transverse Medial condylar Dural Medial side Lateral side
LEFT MEAN RANGE 10
RIGHT MEAN RANGE
8-13
10.1
8.5
6-13
8.9
16.6 9.8
13-20 8-12
16.1
8-14 6-l 13-19
8.8
6-14
5 3
46 2-5
4.4 2.7
2-6 1.5-4
was measured (Table 1). The diameter of the artery was measured at three positions: at the point of entry to the Cl transverse foramen; at the transverse groove of Cl; and at its dural entry. Five other distances were measured: the distance between the point of dural entry and the midline of the atlantooccipital dura; the distance between the point of direction change of the artery from sagittal to transverse above the Cl transverse foramen and the mastoid tip; the distance between the tip of the Cl transverse process and the mastoid tip; the distance between the point of origin of the posterior meningeal artery and the point of dural entry of the VA, and the distance between the point of origin of the muscular branch above Cl and the point of direction change from sagittal to transverse above the Cl transverse foramen.
RESULTS VERTEBRALARTERY The VA entered the transverse foramen of Cl where it ran in a vertical and slightly anterior direction. Just above the Cl transverse foramen, the artery changed direction dorsally and ran farther in the sagittal plane. In most cases this change of direction was associated with an acute angle, but in others it was in a posteromedial direction. Then the artery changed direction again and ran transversely above the posterior arch of Cl. The distance between the mastoid tip and the point of direction change of the artery from sagittal to horizontal was 2 1 mm (mean) on the left side (12-30-mm range) and 21.2 mm (mean) on the right side (12-30-mm range) (Figure 2). This part of the artery ran a straight or arched course depending on the length and direction of the second segment of the artery. If the length of the second part was long the artery ran in a straight course, and if it was short the artery ran in an arched course with posterior protrusion above the Cl posterior arch. This posterior
394
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of atlantal part of qtweenVADrawing showing: distance bemastoid tip and VA; mastoid tip and tip of Cl transverse process; distance between point of dural entry and midline of atlanto-occipital dura (from Lang with modification, 39).
protrusion of the artery was 11 mm in one specimen. In this situation the artery could be injured during some operations at the craniocervlcal junction. This part of the artery related anteriorly to the lateral mass of the atlas and atlanto-occipital joint. It passed in the transverse groove above the Cl posterior arch to the point of direction change from transverse to vertical at the medial side of the lateral mass of the atlas and occipital condyle. The direction change usually occurred at the end of the transverse groove medially but in one specimen it changed its direction in the middle of the groove. The artery then passed upward and medially, partially covered by the atlanto-occipital membrane, and entered the dura at the lateral aspect of the foramen magnum. At that part of the artery, the dura formed a funnel-shaped sheath around the artery. The length of this sheath was longer medial to the artery than lateral to it. The distance between the point of dural entry and the midline of the atlantooccipital dura was 16.8 mm (lo-19.5-mm range) (Figure 2). The diameter of the artery was found to be 4 mm on the left side (2.5~6-mm range) and 3.9 mm on the right (2.3-5.5-mm range); there was no change of the artery diameter in its atlantal part (Table 2). The Cl transverse process has an important role in the approach to this part of the VA. It is the most prominent transverse process of the cervical spine and can be palpated subcutaneously halfway between the mastoid tip and the angle of the mandible. The distance between the tip of the Cl transverse process and the mastoid tip was measured. On the left side it was 21 mm (15-30-mm range), on the right side, 18.8 mm (1 l-25-mm range) (Figure 2).
BRANCHES As the artery entered the transverse foramen of Cl, it formed a radiculomuscular branch below the Cl posterior arch that ran medially to the atlantoaxial joint anteriorly and C2 nerve inferiorly. This branch was found in all specimens. It divided into a dural branch that entered the dura with the C2 nerve and muscular branches. This radiculomuscular branch originated just at the point of entry of the VA to the Cl transverse foramen, but in one case it originated at the lower part of the foramen (Figure 3). Above the Cl posterior arch the artery formed another muscular branch directed posterosuperiorly and medially. This branch was found in four specimens. The point of origin of this artery was 5-10 mm distal to the point of the VA direction change from sagittal to transverse above the Cl posterior arch (junction between sagittal and transverse segments) (Figures 3 and 4). Distal to this branch the VA projected another branch from the posteromedial aspect, the posterior meningeal artery. It traversed a tortuous course to enter the dura. The point of origin of this artery was 7-l 1 mm proximal to the point of dural
q
Diameter of Vertebral Ariery (mm) SIDE
Left Right Left greater than right Right greater than left Left equal to right
MEAN 4
3.9
’ RANGE 2.5-6 2.3-5.5
42.9% 35.7%
21.4%
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395
(A): Atlanta1 part of VA showing C2 nerve going 1 (A): Sagittal and transverse of atlantal part of VA. q(RMbr)around Cl-C2 part of VA. Radiculomuscular branch 0 Muscular branch (Mbr), periosteal sheath (PSh), at entry to Cl transverse foramen, muscular venous plexus (VP), and Cl posterior arch. (3): Drawing
branch (Mbr) from transverse part, occipital condyle (OcC), Cl (Cl) posterior arch, transverse process (‘fP>, and atlanto-occipital membrane (AOcM). Cl transverse foramen is opened posteriorly and part of the posterior arch of atlas is removed. (B): Drawing of previous figure.
entry of VA. This artery was found on the left side in
four specimens, on the right in six, and absent in four. The posterior spinal artery originated at the posteromedial part of the artery at the point of the dural entry. It was found on the left side in four specimens, and on the right in five (Table 3). VERTEBRAL VENOUS PLEXUS The VA was surrounded by a plexus of veins, continuous with the condylar emissary vein above and with veins below the Cl posterior arch around the C2 nerve and the radicular branch of the VA below. This plexus
drained
into two venous
channels
that
accompanied ramen of Cl. or posterior the foramen
the artery through the transverse foThese two veins were lateral, medial, but never anterior to the artery inside (Figure 5).
of previous figure.
PERIOSTEAL SHEATH The artery and part of the venous plexus were surrounded by a periosteal sheath that encircled the whole course of the artery up to the point of dural entry, where it adhered to the dura mater. This sheath was calcified, converting the transverse groove into a complete tunnel in three specimens, and into a partial tunnel in four specimens (Figure 6).
q
Branches of the Atlanta1 Part of Vertebral Artery NUMBER BRANCH
Radicufomuscular Muscular Postmeningeal Postspinal
PERCENTAGE
LEFT
RIGHT
LEFT
RIGHT
14 4 4 4
14 4 z*
100 28.6 28.6 28.6
100 28.6 42 35.7
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(A): Transverse segment of atlantal part of VA after opening periosteal sheath (PSh) showing venous plexus (VP) surrounding the artery (VA), and Cl posterior arch (Cl). (B): Drawing of previous figure.
Cl
NERVE
The Cl nerve exited the dura medial to the artery through the funnel-shaped dural opening. It continued downward and laterally to run inferior and slightly anterior to the artery in the transverse groove. At the transverse groove the nerve branched around the artery to supply the muscles of the posterior triangle of the neck. As the VA enters the Cl transverse foramen the nerve continued anteriorly to the artery and divided into muscular branches (Figure 7).
(A): Transverse of atlantal part of VA, showing calq(Cal.m PSh). cification of periosteal sheath around the artery (B): Drawing of previous figure.
DISCUSSION Within the long history of vascular surgery, the vertebral artery has a small place due to its deep location and difficult access for exploration. Sanson (1836) stated that the VA is beyond the reach of surgery. Since that date many surgeons have suc-
ceeded in operating on the VA, starting with Maisonneuve (1853) who first successfully ligated the first portion of the vertebral artery. Later Fenger (1881) performed a successful ligation on the third
Microsurgical
Anatomy of the Vertebral Artery
B (A): Atlanta1 part of VA after removal of foraminaf, sagittal, and half the transverse segment, showing Cl nerve (Cln) as it goes anteroinferior to artery and continues laterally to supply muscles in this area. It also shows condylar vein (CV), Cl posterior arch (Cl), Cl transverse foramen (TP), Cl transverse process, venous plexus (VP) and occipital condyle (OcC). (B): Drawing of previous figure.
part of the artery when he treated a traumatic aneurysm in a 19-year-old man [ 111. In 1888 Matas described the first operation on an aneurysm of the distal part of the artery using a posterior approach [22]. Following this, ligation of the artery was proposed in different cases with various indications: epilepsy (2) brain tumors (7) and arteriovenous fistulas (8). A major advance in the diagnosis of VA diseases was made after the introduction of angiography [23]. Nevertheless, until the end of the 1950s surgery of the VA remained directed to arteriovenous fistulas and aneurysms of traumatic origin. In 1959 Cate and Scott performed the first endarterectomy of the proximal VA [6]. Following the development of vascular surgery, a better understanding of the role of the VA in cerebral ischemia, and improvement in surgical techniques, preservation
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397
and revascularization of the VA contributed to more effective surgical intervention in this region. Artery diameter in our specimens was 4 mm on the left side and 3.9 mm on the right. Francke and coworkers found arterial diameters of 4.7 mm on the left side and 4.3 mm on the right [9]. The vertebral arteries are frequently asymmetric. Sometimes the minor VA is too small to be detected by angiography, and it may end in the posterior inferior cerebellar artery. If this minor VA ends in the basilar trunk it is termed hypoplastic; if it is not connected to the basilar artery it is termed atretic. Sometimes the artery may be completely absent. In that case it is frequently replaced by persistent congenital anastomoses [35]. There are four possible persistent congenital anastomotic arteries, and three of them are intracranial: the trigeminal, otic, and hypoglossal. One, the proatlantal, is extracranial. They represent persistent embryonic anastomotic arteries between the carotid and basilar circulatory systems. The proatlantal is a rudimentary channel that forms the proximal portion of the occipital artery. The occipital artery originates from the internal carotid and connects later with the external carotid artery. This explains why two types of proatlantal arteries may be observed, one arising from the external carotid and the other from the internal carotid. In both types, the artery forms a sharp curve after its origin to rest upon the supe rior aspect of the transverse process of Cl. It does not pass through the transverse foramen of any vertebra before entering the skull through the foramen magnum, since it joins the normal course of the VA. In case of a persistent proatlantal artery, the vertebral artery is absent or hypoplastic. This suggests that the proatlantal artery persists because of the failure of normal vertebral artery development [ 18,19,27,29,34,35]. Another anomaly of the VA is duplication or fenestration of the artery. This is extremely rare in persons of Western European descent, but in Japanese people it is present in 1% of patients. It occurs predominantly in the upper cervical region and is associated with other intracranial anomalies. It occurs when a primitive segmental artery persists during the embryologic development of the artery. With duplication, either the main trunk penetrates the dura at the Cl-C2 levels and the atretic or hypoplastic trunk follows the normal course, or there are two trunks of equal size, one extradural and the other intradural. This may cause an acute subdural hematoma and death, following lateral cervical spine puncture [30,36,37]. Calcification of the periosteal sheath around the artery is a common finding. Oliveria and colleagues
398
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reported that 28% of their cases had a complete canal, 24% had a partial canal, and 48% had a shallow groove [25]. Lamberty and Zivanovic reported in their series that 15% had a complete canal, 22% had a partial canal, and 63% had a shallow groove [ 151. Radojevic and Negovanovic found a bony canal bilaterally in 7% of cases, unilaterally in 14%, and an incomplete bony canal in 2% of their specimens [28]. To avoid kinking and subsequent possible brain stem infarction, calcification of the periosteal sheath and tunneling of the transverse groove should be considered during operations requiring mobilization of the artery, especially if the artery is the dominant one. In our study the posterior meningeal artery was found on the left side in four specimens, on the right side in six. The meningeal branches of the VA are usually small, but may become significantly enlarged in a variety of pathologic conditions. Both anterior and posterior meningeal branches arise from the extracranial VA and supply a portion of the dura of the posterior fossa. Newton reported the posterior meningeal artery on the right side in 29.8% of their cases and on the left side in 40% (angiographic study) [24]. This artery originates from the posterior portion of the VA between the arch of the atlas and the base of the skull. The artery courses backwards and upwards toward the posterior rim of the foramen magnum. Its course is slightly tortuous in its proximal extracranial portion. After entering the skull it assumes a straighter course extending superiorly, parallel, and close to the inner table of the occipital bone. It could occasionally be followed to the internal occipital protuberance and, rarely, could be seen extending more superiorly up to the level of the tentorium [24]. We found the posterior spinal artery on the left side in four specimens, and on the right in five. It usually arose from the posteromedial surface of the VA at the point of its dural entry or from the intradural part of the artery [5,25]. In the subarachnoid space, the artery coursed medially behind the most rostra1 attachments of the dentate ligament, and upon reaching the lower medulla it divided into ascending and descending branches. The ascending branch coursed through the foramen magnum and supplied the restiform body, the gracil and the cuneate tubercles, the rootlets of the accessory nerve, and the choroid plexus near the foramen of Magendie, and may have given off branches which anastomosed with branches of the posterior inferior cerebellar artery. The descending branch passed downward on the posterolateral surface of the spinal cord between the dorsal rootlets and the dentate ligament. It anastomosed with the posterior
Abd El-Bary et al
branches of the radicular arteries that entered the vertebral foramen at lower levels. The descending branch gave off collateral branches, each lower one being smaller and less constant than the previous one. They coursed medially across the posterior surface of the spinal cord and joined to form an artery located in the midline, parallel to the posterior spinal arteries [25]. The posterior inferior cerebellar artery (PICA) is the largest branch of the vertebral artery; it has a variable site of origin from the foramen magnum to the vertebrobasilar junction. Akar et al found the artery to originate 16.4 mm (3.0-25.0 mm) from the vertebrobasilar junction; none of the PICA originated below the foramen magnum in their study [ 11. However, Lister et al reported the origin of the PICA below the foramen magnum in 7 out of 42 PICAS, and the origin was located 16.9 mm from the vertebro-basilar junction (o-35.0 mm range) [20]. Margolis and Newton [21] found the origin of the PICA between 24 mm below and 45 mm above the foramen magnum. In their study, 18% of PICAS originated below the level of the foramen magnum, 4% at the level, and 57% above the level of the foramen magnum; the site of origin was 16.0 mm (O-35.0-mm range) from the vertebrobasilar junction. The PICA was noted to present as a single artery in 90% of cases, duplicated in 6%, and absent in 4%. In case of absent PICA, the anterior inferior cerebellar artery branches supply the territory of the PICA. Lister et al divided the PICA into five segments: the anterior medullary segment in front of the medulla; the lateral medullary segment, which courses beside the medulla and extends to the origin of the glossopharyngeal, vagal, and accessory nerves; the tonsillomedullary segment, which courses around the caudal half of the cerebellar tonsil; the telovelotonsilar segment, which courses in the cleft between the tela choroidea and the inferior medullary velum rostrally and the superior pole of the cerebellar tonsil caudally; and the cortical segment, which runs over the cerebellar surface [20]. The Cl nerve was found in all cases to exit the dura medially to the artery, moving anteromedially to the artery down to the transverse groove, then inferiorly and slightly anteriorly to the artery in the transverse groove of Cl. It continued anteriorly to the artery as it entered the transverse foramen of Cl. The Cl nerve was formed mainly of anterior root. The posterior root was inconstant and was variably found to be intimately related to the presence or absence of connection with the spinal nerve. Ouaknine and Nathan reported the absence of Cl posterior root in 64% of their specimens [26].
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Anatomy of the Vertebral Artery
There are various possibilities of nerve supply in areas normally innervated by the Cl posterior root, as well as the central course of the sensory fibers of Cl. These possibilities include a normal course through the Cl posterior root and connection with the accessory nerve via anastomosis. The central fibers still reach the medulla and spinal cord, passing directly into the posterior root, although it is possible that some fibers reach the medulla with the accessory nerve. Other possibilities are that sensory fibers reach the medulla through the rootlets of the 11th cranial nerve (almost half of all specimens), and the rest take over the corresponding area of Cl by C2 rootlets that will reach the spinal cord by the same nerve root or by the 11th cranial nerve. The Cl posterior root participates in the innervation of the meninges, the atlanto-occipital joints, and the area of the occipital for-amen [26]. The neurosurgical significance of Cl posterior rootlets becomes apparent in neurotomy operations. Including these rootlets in radiculotomy will avoid residual pain after sectioning C2 and C3 dorsal roots in cases of lesions causing intractable pain at the craniocervical junction [26]. The atlantal part of the VA can be approached by different routes: lateroanterior, dorsolateral [ 131, and posterior [3]. The lateroanterior approach is recommended by many authors [ 10,12,14,32,33, 38,39,40]. It provides relatively easy access to any part of the VA, from its ostium up to the intracranial portion, which is wide and safe. This approach passes through the anatomic plane between the sternocleidomastoid muscle and the internal jugular vein without any vessel to dissect. The only element crossing the field in this approach is the accessory spinal nerve that has to be freed. In addition, numerous other structures can be controlled by the lateroanterior approach including the carotid artery, cervical nerve roots, hourglass tumors, and vertebral bodies. Hemilaminectomy of Cl and C2, hemicraniectomy, and infratemporal ap proaches follow the same technique as the lateroanterior approach [ 111. The importance of controlling the VA without opening the periosteal sheath must be stressed to avoid problems with the perivertebral venous plexus. Moreover, with periosteal dissection the VA is protected surgically. There are two sites that need particular attention. The first is the curvature of the VA when it leaves the groove of the atlas to join the dura mater. There are two identifying landmarks of this site: change in height of the posterior aspect of the atlas, which increases just medially to this point, and a muscular branch (the suboccipital artery), which originates at this point. The second site is the dural penetra-
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tion of the VA. It is not advisable to free the artery completely at this level, since the periosteal sheath is particularly adherent to the dura mater. It is safer to cut the dura mater around but at some distance from the VA [ 121. The muscular branch above the posterior arch of the atlas is usually harvested during exposure of the artery, and care must be taken not to confuse the VA with the posterior inferior cerebellar artery that may rarely originate from the extradural VA [16,17,20,31,41]. REFERENCES 1. Akar ZC, Dujovny M, Slavin KV, Gomez-Tortosa E, Ausman JI. Microsurgical anatomy of the intracranial part of the vertebral artery. Neurol Res 1994;16:17180. 2. Alexander W. The treatment of epilepsy by ligature of the vertebral arteries. Brain 1882;5:170-87. 3. Ausman JI, Diaz FG, Pearce JE, de 10s Reyes RA, Leuchter W, Mehta B, Pate1 S. Endarterectomy of the vertebral artery from C2 to posterior inferior cerebellar artery intracranially. Surg Neurol 1982;18:400-4. 4. Caplan LR. Vertebrobasilar system syndromes. In: Vinken PJ, Bruyn GW, Klawans, eds. Handbook of clinical neurology. Vascular disease. Part 1. Amsterdam: Elsevier Science Publisher B.V, 1988;53:371-409. 5. Carpenter MB. Neuroanatomy. 4th ed. Philadelphia: Williams and Wilkins, 1991:449. 6. Cate WR, Scott HN. Cerebral ischaemia of central origin: relief by subclavian vertebral artery thromboendarterectomy. Surgery 1959;45:19-31. 7. Dandy WE. Intracranial arterial aneurysm. Ithaca: Comstock Publishing Co., 1944. 8. Elkin DC, Harris MH. Arteriovenous aneurysm of the vertebral vessels: report of ten cases. Ann Surg 1946; 124:934-51. 9. Francke JP, Diemarino V, Pannier M, Argenson C, Libersa C. The vertebral arteries. The V3 atlanto-axial and V4 intracranial segments collaterals. Anat Clin 1981;2:229-42. 10. George B, Laurian C. Surgical approach to the whole length of the vertebral artery with special reference to the third portion. Acta Neurochir (Wien) 1980;51: 259-72. 11. George B, Laurian C. The vertebral artery. In: Pathology and surgery. New York: Springer-Verlag, 1987;117:146-50. 12. George B, Dematons C, Comphignon J. Lateral approach to the anterior portion of the foramen magnum: application to surgical removal of 14 benign tumours: technical note. Surg Neurol 1988;29:484-90. 13. Gilsbach JM, Eggert HR, Seeger W. The dorsolateral approach in ventrolateral craniospinal lesions. In: Textbook of diseases in the crania-cervical junction. New York: Walter de Gruvter, 1987:369-73. 14. Jonson RM, Murphy MJ, Southwick WO. Surgical approach to the spine. In: Rothman RH, Simeone FA, eds. The spine. Philadelphia: W.P. Saunders Co, 1992: 1607-33. 15. Lamberty BGH, Zivanovic S. The retro-articular vertebral artery ring of the atlas and its significance. Acta Anat 1963;85:113-22.
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16. Lang J. Clinical anatomy of the head: neurocranium, orbit and craniocervical regions. New York: SpringerVerlag, 1983:360,420,432. 17. Lang J. Contents of the posterior cranial fossa. In: Clinical anatomy of the posterior crania1 fossa and its foramina. New York: George Thieme-Verlag, 1991:1644. 18. Lasjaunias P, Theron J, Moret J. The occipital artery: normal anatomy, arteriographic aspects, embryological significance. Neuroradiology 1978;15:31-7. 19. Lie TA. Congenital malformations of the carotid and vertebral arterial systems including persistent anastomosis. In: Vinken PJ, Bruyn GW, eds. Handbook of clinical neurology. New York: Elsevier, 1972;12:289339. 20. Lister JR, Rhoton AL, Matsushima T, Peace DA. Microsurgical anatomy of the posterior inferior cerebellar artery. Neurosurgery 1982;lO: 170-99. 21. Margolis MT, Newton TH. The posterior inferior cerebellar artery. In: Newton TH, Potts DG, eds. Radiology of the skull and brain: angiography. Book 2. St Louis; CV Mosby, 1974;2:i710-74. 22. Matas R. Traumatisms and traumatic aneurysms of the vertebral artery and their surgical treatment with report of a cured case. Ann Surg 1893;18:477-516. 23. Moniz E. L’enc ephalographie art ereille, son importance dans la localisation des tumeurs c er ebrales. Rev Neurol 1927;2:72-81. 24. Newton TH. The anterior and posterior meningeal branches of the vertebral artery. Radiology 1968;91: 271-79. 25. Oliveria E, Rhoton AL, Peace D. Microsurgical anatomy of the region of the foramen magnum. Surg Neurol 1985;24:293-352. 26. Ouaknine G, Nathan H. Anastomotic connections between the eleventh nerve and the posterior root of the first cervical nerve in humans. J Neurosurg 1973; 38:189-97. 27. Parkinson D, Reddy V, Ross RT. Congenital anastomosis between the vertebral artery and internal carotid artery in the neck: case report. J Neurosurg 1979;51:697-99. 28. Radojevic S, Negovanovic B. Lagottiere et les anneuaux osseaux de I’atlas. Acta Anat 1963;55:186-94. 29. Rao TS, Sethi PK. Persistent proatlantal artery with carotid vertebral anastomosis: case report. J Neurosurg 1975;43:499-501. 30. Rogers LA. Acute subdural hematoma and death following lateral cervical spine puncture: case report. J Neurosurg 1983;58:284-86. 31. Samii M, Knosp E. Approaches to the clivus: approaches to no man’s land. New York: SpringerVerlag, 1992:117-9,126. 32. Sen CN, Sekhar LN. An extreme lateral approach to the intradural lesions of the cervical spine and foramen magnum. Neurosurgery 1990;27:197-204. 33. Shucart WA, Kleriga E. Lateral approach to the upper cervical spine. Neurosurgery 1980;6:278-81. 34. Tanaka Y, Hara H, Mamose G, Kobayaschi S, Sugiat K. Proatlantal intersegmental artery and trigeminal artery associated with an aneurysm. J Neurosurg 1983; 59:520-23. 35. Tasi FY, Mahon J, Woodruff JV, Roach JP. Congenital absence of bilateral vertebral arteries with occipital
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COMMENTARY This article by T. H. Abd El-Bar-y and associates is an important adjunct to our knowledge of the anatomy of the craniocervical junction area. It provides many precise details and measurements about the relationships of the vertebral artery and the neighboring structures. The upper cervical vertebral artery is a key which provides many possibilities for approaching several different areas: the upper cervical spine, the foramen magnum, and the foramen jugulare. Being able to expose and control the vertebral artery permits one to treat lesions directly involving this vessel, such as tumors (osseous tumors, sarcomas, extradural Cl or C2 neurinomas, extradural meningiomas), craniocervical junction malformations, or infectious processes. In these lesions, generally the entire length of the third vertebral artery segment between C2 and the dura has to be exposed, and sometimes transposed. Vertebral artery control improves or provides access to intradural lesions of the foramen magnum to the odontoid
and anterior
arch of the atlas, and to the
foramen jugulare. Obviously, it also allows one to suppress the vascular supply of tumors such as paragangliomas, or to treat arteriovenous fistulae, though endovascular
techniques
most often make it
useless. Finally, the Cl-C2 segment of the vertebral artery is the site of choice for distal revascularization in case of proximal flow compromise (ostial occlusion) or risk of embolism from vascular lesions (aneurysm) and endovascular treatments. All these surgical techniques are quite reliable, providing adequate exposure of the vertebral artery is achieved [ 1,2,3 1. One very important point stressed by the authors is the periosteal sheath surrounding
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Surg Neurol 1995;44:392-401
the vertebral artery and the venous plexus. In all cases, the vertebral artery must first be controlled out of this periosteal sheath to avoid any troublesome bleeding from the venous plexus. If the vessel wall has to be controlled (for instance, to perform a venous bypass), the sheath is opened in a second step. The control of the vertebral artery requires perfect knowledge of the anatomy of this vessel, with all possible variations and anomalies. Dr. Abd El-Bary and his colleagues must therefore be thanked for the anatomic details given in their article, of which any surgeon
working in the region of the craniocervical tion should be aware. Bernard
VERY GUN THAT IS FIRED, EVERY WARSHIP LAUNCHED, EVERY ROCKET FIRED, SIGNIFIES, IN THE FINAL SENSE, A THEFT FROM THOSE WHO HUNGER AND ARE NOT FED, THOSE WHO ARE COLD AND ARE NOT CLOTHED. THE WORLD IN ARMS IS NOT SPENDING MONEY ALONE. IT IS SPENDING THE SWEAT OF ITS LABOURERS, THE GENIUS OF ITS SCIENTISTS, THE HOPES OF ITS CHILDREN. GENERAL,
junc-
George, M.D. Paris, France
REFERENCES 1. George B, Laurian C. The vertebral artery: pathology and surgery. New York: Springer Verlag, 1987. 2. George B, Lot G, Velut S. Tumors of the foramen magnum. Neuorchirurgie 1993;39:1-92. 3. George B, Laurian C. Impairment of vertebral artery flow caused by extrinsic lesions. Neurosurgery 1989; 24:206-14.
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DWIGHT D. EISENHOWER (1890-l 969) REPUBLICAN POLITICAN, PRESIDENT SPEECH, APRIL 1953