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10
the artery, partially enclosed in a bony gutter between the
anterior and posterior tubercles of each cervical transverse
process. Venous tributaries and arterial branches are abounding at the level of the intertransversal spaces; consequently, a
better and bloodless approach to the VA is obtained with partial bone excision with a rongeur, in the bony canal rather
than between the transverse processes. Extensive exposure of
the VA can be necessary in patients with a shorter neck or
with stenoses beyond the very origin of the artery. While performing the deep cervical plexus block and in order to avoid
the inadvertent puncture of the VA, contact with bone represents a good guiding maneuver.
The transverse foramina of the atlas (C
1
) are located more
laterally than those of the axis (C 2 ): at this level, the VA
depicts a divergent lateral and posterior course. The artery
winds around the lateral masses of the atlas; pierces the posterior atlanto-occipital membrane and, shortly afterward, the
dura mater, entering the skull through the occipital foramen;
and shifts from a posterior location to an anterior position
(Fig. 1.15 ). At the level of the pons, the two vertebral arteries
converge and form the basilar trunk. The tortuosity of the
distal cervical (extracranial) VA allows the extensive and
complex movements of the neck. This segment of the VA is
contained in the triangular space bounded by the suboccipital muscles delimitated by the rectus capitis posterior major
(medially), obliquus capitis superior (superiorly and laterally), and obliquus capitis inferior (inferiorly and laterally).
The triangle lies deep to the semispinalis capitis and trapezius muscles. A strict posterior approach to this segment of
the VA is more demanding for the surgeon being performed
only when an associated opening of the posterior cranial
fossa is also contemplated.
Not infrequently, the left VA has a separate origin, at the
level of the aortic arch, between the origin of the left carotid
and the left subclavian arteries. This variation must be sought
and identifi ed during angiographic examination. Numerous
other variations of the origin, tract, and termination of the
VA have been reported [
27 – 33 ].
The carotid and the vertebral arteries are divided for practical (clinical, diagnostic, and surgical) reasons in various
segments. A brief presentation and description of these segments are mandatory, before illustrating the surgical
approaches to aforementioned arteries.
1.1.2.7 The Segments of the Carotid Artery
The left CCA has an intrathoracic part as it originates from
the aortic arch (normally) or from the brachiocephalic trunk
or from a common carotid trunk (the most common variations
of origin). The artery is located in the superior mediastinum
before reaching the base of the neck. The left phrenic nerve
comes into close contact with the left CCA at its aortic origin; the left laryngeal recurrent nerve lies between the left
subclavian and the CCA. The trachea and the brachiocephalic trunk are on the right side of the left CCA.
The cervical segments of the right and left CCAs show
similar disposition and relationships while depicting an
oblique and lateral course in the neck toward their
bifurcation.
1.1.2.8 The Segments of the Internal Carotid
Artery (Fig.
1.16 )
The ICA may be divided for clinical, surgical, and diagnostic
purposes in the following segments: cervical, petrous, cavernous, cisternal, and cerebral.
• The cervical segment begins at the level of the bifurcation,
terminating as the artery enters the carotid canal. The ori-
gin and the initial part of the ICA can be easily approached;
surgical access to the distal cervical portion of the internal
carotid artery (i.e., above the digastric and stylohyoid
muscles) requires additional maneuvers (see below).
• The petrous segment is contained in the carotid canal of
the petrous temporal bone. The internal carotid artery
curves anteriorly and medially. After leaving the bony
canal, it enters the cranial cavity running upward and
medially above the fi brocartilage that fi lls the foramen
lacerum. Finally, it passes between the lingula and the
petrosal process of the sphenoid bone. The artery can be
approached at this level only by drilling the temporal
bone.
• The cavernous part is covered by the lining endothelium
of the sinus. The artery ascends toward the posterior cli-
noid process, passes on the side of the body of the sphe-
noid bone then turns anteriorly and passes lateral to the
sella turcica. The artery then bends sharply back on itself
under the root of the anterior clinoid process, pointing
thus directly posteriorly (the carotid bend).
• The cisternal segment : after emerging from the cavernous
sinus, the carotid artery penetrates the dura mater medial
to the anterior clinoid process and passes under the optic
nerve.
• The cerebral (terminal) part : the internal carotid artery
ascends in the subarachnoid space up to its point of
division, participating in the formation of the arterial
circle (Willis). Four important arterial branches arise at
the level of the terminal part of the internal carotid artery:
the anterior communicating artery and the middle cere-
bral artery, which represent the so-called terminal
branches, plus the posterior communicating artery and the
anterior choroidal artery.
The ophthalmic artery gives off the central artery of the
retina – that can be easily and directly examined through
ophthalmoscopy, offering important details on the intracerebral circulation. Branches of the ophthalmic artery
anastomose with the angular artery, a branch of the facial
artery establishing thus an important communication
between the internal and the external carotid arteries. The
H. Muresian
11
direction of blood fl ow through this anastomosis can be
easily demonstrated during the Doppler examination and
offers important details on the intracerebral collateral
fl ow between the left and right carotid arteries, also
refl ecting the degree of severity and hemodynamic signifi cance of ICA stenosis.
Various classifi cations were elaborated during time, emanating from different premises and aiming distinct scopes.
The Fisher classifi cation (in retrograde fashion) addressed the
early angiographic imaging requests for localization of
regional tumor pathology and its effects on the ICA [
34 ]. The
following classifi cations addressed especially the intracranial
aneurysms: Gibo et al. [ 35 ], Bouthillier et al. [ 36 ], and, later,
the interest in microsurgical approaches and techniques
focused on the intracranial ICA by Ziyal et al. [ 37 ]. Other
more refi ned classifi cations emphasized the embryologic origins of the various segments of the ICA addressing all manner of cerebrovascular development and variation: Lasjaunias
and Santoyo-Vazquez [ 38 ]. The classifi cation of Bouthillier
et al. which is most widely used nowadays is presented synthetically: C1, cervical; C2, petrous; C3, lacerum; C4, cavernous; C5, clinoid; C6, ophthalmic; and C7, communicating.
Fisher’s classifi cation was limited by its less accurate anatomical details and not least, because segments were numbered opposite the direction of blood fl ow. Although widely
used, the Bouthillier’s classifi cation was challenged by Ziyal
et al. who did not recognize a distinct lacerum segment of the
ICA. The endovascular (and angiographically based) classifi cation system provided by Shapiro et al. [ 39 ] comprises seven
segments of the ICA without alphanumeric correspondence:
cervical, petrous, cavernous, paraophthalmic, posterior communicating, anterior choroidal, and terminus (and may serve
better endovascular purposes). The classifi cations are not
absolute as various diseases (and especially aneurysms) modify the local anatomical relationships. The variation of origination of the meningohypophyseal trunk, of the ophthalmic
artery, etc., may render such partitions forced or artifi cial.
Some of the emerging branches of the ICA may not be evident on angiogram (e.g., the caroticotympanic branch) and
other landmarks also (the precise location of the petrolingual
ligament, the location of the proximal dural ring, and so
forth). The classifi cations contemplating the embryological
framework have a limited surgical or endovascular relevance,
and there is no single all-encompassing classifi cation serving
all purposes.
The segments of the vertebral artery (Fig. 1.17 ). The
widely used and practical classifi cation is reported here
[ 40 , 41 ]:
• V0 = origin . The very origin of the vertebral artery is
sometimes called the V0 segment. The purpose of
assigning a separate name to this portion of the vertebral
artery arises from the need for drawing attention toward
the adjacent parts of the subclavian artery and of the aortic
arch also (in cases with aortic origin of the VA); lesions of
these closely related arterial segments may limit, modify,
or even contraindicate surgical or endovascular approaches.
• V1 = pretransversal or extraosseous . This is the portion of
the vertebral artery most accessed in surgery. From its origin the VA ascends in the solid angle between the anterior
scalene and longus colli muscles. It is covered by the vertebral vein. With older age or atherosclerotic disease, the
V1 portion can show signifi cant kinking. This is the portion of the vertebral artery that can be mobilized most,
allowing, for example, its reimplantation in the common
carotid artery or in the subclavian artery. This portion of
the vertebral artery can be sometimes confused with the
inferior thyroid artery. This latter structure lies however
on a more superfi cial plane (anterior to the vertebral
artery), crosses almost transversally behind the CCA
from lateral to medial, and, characteristically, gives off
numerous cervical branches. Another important detail is
that the vertebral artery is the fi rst (the most proximal)
branch of the subclavian artery.
• V2 = interosseous . The VA passes through the transversal
foramen of the fi rst six cervical vertebrae. The roots of the
cervical spinal nerves and the spinal ganglion are situated
posterior to the VA. Surgical access to this part is more
striving for the surgeon due to the need for partial bone
resection. Exposure between the transverse processes is
even more diffi cult due to the numerous venous tributaries and arterial muscular branches. Lesions of this portion
of the VA can be however treated more conveniently and
more rapidly, by using endovascular techniques and
approaches. The vertebral artery is accompanied by a
plexus of veins and by sympathetic nerves derived from
the cervical ganglia, the latter forming the vertebral nerve.
This segment of the vertebral artery gives off branches to
the cervical nerves, vertebrae, intervertebral joints, neck
muscles, and spinal branches for the cervical spinal cord.
A prominent branch at C5 level anastomoses with the
anterior spinal artery. The anastomoses with the deep cervical and with the ascending cervical artery can become
conspicuous and offer parallel arterial pathways toward
the distal VA (V3 segment). Conversely, such welldeveloped anastomoses may promote the steal syndrome
even in case of occlusion of the vertebral artery at its origin (V0 and V1 segments).
• V3 = distal extracranial segment or the atlas loop . The
artery runs laterally and then vertically toward the
transverse foramen of the atlas (C 1 ); after passing through
the foramen, the artery winds medially along the lateral
mass of the atlas, pierces the posterior atlanto-occipital
membrane, entering the dura mater and the arachnoid at
the level of the foramen magnum. The suboccipital
portion of the vertebral artery from the transverse foramen of the axis (C
2
) to the posterior atlanto-occipital
membrane is a relatively long segment, allowing a proper
1 The Cerebral Circulation
12
surgical exposure for a bypass at this level. Numerous
muscular and articular branches must be identifi ed and
interrupted, at this level.
• V4 = intracranial/intradural . This segment of the verte-
bral artery lies entirely in the subarachnoid space. Before
the confl uence of the two VAs, each gives off some
important branches in the intracranial portion: the posterior spinal artery, the posterior inferior cerebellar artery
(PICA), and the anterior spinal artery. A lower (i.e., more
proximal) origin of the PICA may impede surgical
maneuvers at the level of the intracranial vertebral artery.
1.1.2.9 The Anatomical Variations
of the Vertebral Artery
Variations of the Origin of the VA The most frequently
cited variation is the aortic origin of the left VA (this actually
represents a variation of the branches of the aortic arch), and
the most common site is between the left CCA and the left
SCA; rarely the left VA can originate distal to the left
SCA. The right VA may originate from the ascending aorta,
between the right SCA and CCA (or bicarotid trunk – in the
absence of the brachiocephalic trunk), between the left CCA
and the left SCA, or even distal to the left SCA. With leftsided origin of the right VA, the artery depicts a retroesophageal course [
42 ]. Rarely, a bilateral origin of the VA is also
reported [ 43 , 44 ]. The VA may originate distal to the thyro-
cervical trunk, from the thyrocervical trunk, costocervical, or
from the inferior thyroid artery. Alternatively, the VA may
give off the inferior thyroid artery. These subclavicular variations of origin may mislead the surgeon; more distal exposure of the VA toward the C6 transverse foramen is mandatory
for a correct identifi cation of the VA. Rarely, the VA may
originate from the CCA, ECA, or ICA.
Variations of the Interosseous/Transversal Segment (V2) The
VA may enter any of the transverse foramina from C
7
to C 3 ; when
entering the upper cervical foramina, the VA has a pretransversal
course, underneath the longus colli muscle being more exposed to
injury during anterior approach to the cervical spine. Rarely, a
fi brous band may intermittently compress the VA in extension of
the neck. The VA may depict various types of loops, either at the
level of the intervertebral disks or bodies, sometimes favored by
the growth of osteophytic spurs. Fenestrations of the VA may also
occur at this level (Fig.
1.18 ).
Variations of the Suboccipital Segment (V3) Duplications
and fenestrations occur at C 1 –C 2 level: one part of the VA
follows the usual course, while the second runs intradurally.
The condition when only the latter persists is named “ intra-
dural course of the VA. ” Calcifi cation of the posterior
atlanto- occipital membrane impedes the surgical exposure of
the VA.
Variations of the Intradural/Intracranial Segment
(V4) Fenestrations of this segment are associated with aneu-
rysms and dissections [ 45 ]. The VA may terminate by giving
off the PICA, an occipital branch, or a spinal artery – usually
unilaterally. Bilateral anomalous termination is extremely rare
[ 46 ]. An atretic VA does not join the BT, while the hypoplastic
VA will join the BT however depicting a reduced caliber (less
than 2–3.5 mm) as compared with the major, dominant
VA. Usually, the left VA is dominant. It appears nonetheless
surprising the fact that with vertebral steal syndrome, the two
VAs become of an even caliber, including the V2 segment.
1.2 The Variability of the Territories
of the Major Cerebral Arteries
(Fig.
1.19 )
Contrary to the usually followed schemes depicting the “normal” territories of the major cerebral arteries [ 47 ], a consider-
able interindividual and intraindividual (right-left and
anterior-posterior) variation in the diameter and the volume of
brain vascularized by each of the major artery was demonstrated [ 48 ]. Indeed, the neurodiagnostic of the watershed
ischemia based on the location of the infarct appears to be
more complex, and the templates of relatively unvarying territories of the major cerebral arteries would be most misleading [ 49 ] (Fig. 1.19 ). In addition, each of the individual
territories may change in time as a result of the altering hemodynamic circumstances as well as in stenotic/occlusive arterial
disease [ 50 , 51 ]. A complex interdependence is also demon-
strated between the blood fl ow, the arterial diameter, the resistance of the target tissues, and the volume of distal tissues
vascularized. Moreover, there are well-known differences
between the vascular resistance and blood fl ow of the cortical
gray matter, white matter, and the gray matter of the basal
nuclei. As mentioned before, the cerebral blood fl ow is maintained constant, at approximately 50 ml per 100 g of brain tissue
−1
/min −1 . The mean fl ow in the gray matter is 3.9 times as
high as the fl ow in the white matter, and the mean fl ow in the
basal nuclei is only slightly higher than that in the cortex [
52 ,
53 ]. There is a corresponding higher vascular density in the
gray matter. Regarding the intraindividual variations, the most
conspicuous asymmetry between the calibers of homonymous
arteries was found for the anterior cerebral artery. Consequently,
it appears that one of the most relevant elements of the arterial
circle of Willis [ 54 ] is the anterior communicating artery
(ACommA), and this particular may explain the higher prevalence of aneurysm development at this level [ 55 ]. Not least,
the ACommA has signifi cant branches vascularizing the optic
chiasm, lamina terminalis, hypothalamus, diagonal band of
Broca, cingulate gyrus, genu of corpus callosum, and pillar of
fornix, and injury to these vessels caused either by aneurysmal
rupture or surgical manipulation may lead to serious clinical
defi cits mostly psycho-organic syndromes [ 56 ].
H. Muresian
13
Fig. 1.1 The cerebral veins. Panel ( a ), lateral view of the main cerebral
veins. Sup. Cer. Vv. superior cerebral veins, joining the superior sagittal
sinus ( SSS ). The thalamostriate vein ( TSV ) merges into the great cere-
bral vein of Galen ( GCV ); after joining the basal vein of Rosenthal
( BV ), they form the straight sinus ( StS ). The StS unites with the trans-
verse sinuses ( TrS ) at the level of the confl uence of the sinuses ( CoS ).
The TrSs continue with the sigmoid sinuses ( SyS ) eventually becoming
the internal jugular veins ( IJV ). A conspicuous anastomosis is repre-
sented by the vein of Labbe’ ( Labbe’ ). The approximate position of the
cavernous sinus ( CavS ) is also shown. Panel ( b ), an oblique projection
demonstrating better the confl uence of the sinuses. Panel ( c ), additional
lateral view of the cerebral veins, demonstrating the inferior sagittal
sinus ( ISS ), together with the previously mentioned sinuses (see above).
Panel ( d ), various phases of venous fl ow as seen during a routine angio-
gram. See the legend above for details and abbreviations. Panel ( e ), a
sequential demonstration of the cerebellar veins, eventually draining
into the IJVs. Lateral view
SSS
GCV
StS
SyS
CoS
IJV
CavS
Labbe’
Sup. Cer. Vv.
TSV
BV
TrS
StS
SSS
CoS
TrS
SyS
SSS
ISS
SS
SyS
CoS
IJV
TrS
a
c
b
1 The Cerebral Circulation
14
d
Fig. 1.1 (continued)
H. Muresian
15
e
Fig. 1.1 (continued)
1 The Cerebral Circulation
16
III
II
I
Fig. 1.3 The three surgical zones of the neck. Zone I extending about
1–2 cm superior to the clavicle is represented in violet. It corresponds
roughly to the inferior belly of the omohyoid muscle. The small triangle
between the two heads of origin of the SCM can be also included in this
area. The IJV is readily approachable at this level. Zone II ( light gray )
extends superior to zone I, up to the level of the line continuing the
inferior margin of the mandible. Note that with the head in extension,
zone II appears more reduced posteriorly. Zone III ( yellow ) corresponds
to the cranial base
T
DP - SH
DA
O
S
OI
SCM
SM
D
C
M
Occ
SC
Mast
Clavicle
Fig. 1.2 Schematic representation of the neck triangles. Left side of
the neck with the head in extension and contralateral rotation. DA digas-
tric muscle, anterior belly; DP-SH digastric muscle, posterior belly and
stylohyoid. Mast mastoid process, OI omohyoid inferior belly, OS omo-
hyoid superior belly, SCM sternocleidomastoid muscle (and region). T
trapezius muscle. The triangles are as follows: C carotid, D digastric, M
muscular, Occ occipital, SC supraclavicular, SM submental. The small
supraclavicular triangle formed between the clavicular and sternal
heads of origin of the SCM is fi gured in blue; the IJV (“the inferior
bulb”) lies underneath
H. Muresian
17
Fig. 1.4 The carotid sheath and the cervical fascia. Panel ( a ), the
superfi cial layer of the cervical fascia and the platysma muscle. The
anterior jugular veins ( AJVs ) are also visible. Panel ( b ), part of the
carotid triangle appears superior to the omohyoid muscle ( OI inferior
belly). The omohyoid is covered and retained in its position by the
middle layer of the cervical fascia (visceral or pretracheal layer). The
anterior jugular vein ( AJV ) joins the IJV just underneath the OI. The
external jugular vein ( EJV ) is partially visible in the lateral part of the
image. SCM sternocleidomastoid muscle (cut and retracted). Panel ( c ),
the carotid triangle and the carotid sheath. The dissection proceeds
deeper, superior to the inferior belly of the omohyoid muscle ( OI ). By
opening the sheath, direct access is possible to the common carotid
artery and bifurcation ( CCA ), the internal jugular vein ( IJV ), the cervi-
cal ansa (hypoglossal ansa*). Note the dense tissue of the carotid sheath
(held with pickups). Panel ( d ), further dissection demonstrates the
carotid bifurcation, the vagus nerve ( X ), and the sympathetic trunk ( S );
the latter is covered/contained by the prevertebral layer of cervical fascia (the prevertebral fascia was dissected in order to demonstrate the
sympathetic trunk). Intraoperative image, at the right for comparison
(in the intraoperative image, the sympathetic trunk is not readily visible,
being covered by the pretracheal layer of the cervical fascia). Panel ( e ),
the pretracheal fascia covers the infrahyoid muscles, the thyroid and
parathyroid glands, the trachea, and the larynx. The thyroid gland is
visible, together with the superior and inferior thyroid vessels and the
recurrent laryngeal nerves (Recc). CCA common carotid artery, ITA
inferior thyroid artery (note its transversal course from lateral to
medial), ITV right inferior thyroid vein, X vagus nerve
AJVs
a
1 The Cerebral Circulation
18
OI
SCM
AJV
EJV
OI
OS
IJV
CCA
*
b
c
Fig. 1.4 (continued)
H. Muresian
19
OS
CCA
ICA
ECA
X
IJV
S
IJV
OS
CCA
ICA
STA
X
d
Recc
ITV
ITA
X
CCA
Fig. 1.4 (continued)
1 The Cerebral Circulation