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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
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
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
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
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
Microsurgical
Surg Neurol
1995;44:392-401
-Fs
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
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
Abd El-Bary et al
Surg Neurol
1995;44:392-40 1
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
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%
Microsurgical
Surg Neurol
1995;44:392-401
395
drained
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).
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
396
Surg Neurol
1995;44:392-401
Abd El-Bar-y et al
Cl
NERVE
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
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
Surg Neurol
1995;44:392-401
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
Surg Neuroi
1995;44:392-401
Abd El-Bary et al
Microsurgical
Surg Neurol
1995;44:392-401
399
400
Abd El-Bary et al
Surg Neurol
1995;44:392-401
36.
37.
38.
39.
40.
41
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
techniques
Surg Neurol
1995;44:392-401
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.
U.S.
401
DWIGHT
D. EISENHOWER
(1890-l
969)
REPUBLICAN
POLITICAN,
PRESIDENT
SPEECH,
APRIL
1953