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Carotid Artery Embryology1996 PDF
Carotid Artery Embryology1996 PDF
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The word carotid is derived from the Greek "If you compress the 4 vessels [carotids and
jugulars] of either side where they are in the
KotpaLv, to stupefy. The vessel has also been
thioat, he who has been compressed will sud-
termed the apoplectic or sopornl artery in recog- denly fall to the ground asleep as though dead
nition of the'common effect of compression of and will never wake himself; and if he is left
both carotids. Aristotle is credited as the earli- in this condition for the hundredth part of an
est source of this observation.26 The Greek phy- hour, he will never wake, neither of himself
sician Galen (129-799) laid early groundwork nor with the aid of others."
for the understanding of blood flow by estab-
lishing that arteries contain blood and not air; It was the anatomist Andreas Vesalius
however, he considered the liver to be the pri- (151,4-1,564) who first observed in systematic
mary organ of the vascular system and_ be- detail the human vascular system. His master-
lieved thit blood was delivered to the end or- work, De Humani Corporis Fabrica (1543), is
gans through both arteries and veins.E The considered by some to be the greatest contribu-
circulation of the blood was established by the tion to the medical sciences. This work is based
physician William Harvey (1,578-1.657), who on both animal and human dissections, and
published his revolutionary findings in 1628 his drawings of the vascular system in book
lnExercitotio Aruttomic de Motu C{udis et Sangui- III reflect this experience and his Galenic un-
nis in Animalibus (Analomical Essay on the Mo- derstanding of blood flow (Fig. 1).34
tion of the Heart and Blood in Animals).31 With the acceptance of Harvey's concept of
Early attempts to delineate the structural el- the circulation, understanding of the vascular
ements of the human vascular system date to anatomy improved.3l Details regarding the
the artist and scientist Leonardo da Vinci outflow of the carotids was provided by the
(1.452-1519). His understanding was based on work of the London physician Thomas Willis
a modification of Galenic theory, and his obser- (7627-7675) published in Cerebri anatome
vations were based on dissections of animals nervorumque (166$. The physician and anato-
and a detailed study of a 100-year-o1d human mist Antonio Scarpa (7752-1832) was the first
circa 1504-1506. Although his depiction of the to depict the carotid sinus in Tabulae neurologi-
neck arteries in his famous notebooks does cae adillustrondum historiam anotomicom cardiac-
include the carotid arteries, the details are orum neralrum (1794). The role of variation in
flawed. A notation on his anatomic drawing the vascular tree was explored by the surgeon
of the neck (in his distinctive mirror script) and anatomist Richard Quain (1800-1887),
indicates his understanding of the importance who published the results of dissections of
of the carotids26: nearly a thousand subjects in The nnatomy of
From the Divisions of Neuroradiology (lEH) and Neurosurgery (DHD); Barrow Neurological Institute, St. Joseph's
Hospital and Medical Center, Phoenix, Arizona
the arteries of the human body with its applications are present by 28 days, but the first two arches
to pathology and operntiae surgery in lithographic involute before formation of the fifth and sixth,
drawings with practical commentaries (7844). so that the arches are not all present at any
These investigators and others set the stage one time.28 The pattern of persistence or regres-
for the radiographic evaluation of the carotid sion of these arches is reflected in the normal
arteries in the living patient, which was made anatomy and anatomic variations of the
possible by the techniques of angiography dis- great vessels.
cussed by Egas Moniz in his classic workL'An- The first two paired aortic arches involute
giogr nphie Cerebr nle (1934).'?1 without a significant remnant in the adult vas-
culature. The third arches are precursors to the
carotid system, and the fourth arches develop
EMBRYOLOGY asymmetrically. The left fourth aortic arch re-
mains in continuity with the aortic sac and
The embryologic vascular system develops left dorsal aorta, forming the normal adult left
immediately before the appearance of so- aortic arch. The right fourth arch, together with
mites, at approximately 19 days. Primitive part of the right dorsal aorta, forms the proxi-
spongy mesoderm, mesenchyme, forms vas- mal right subclavian artery. The fifth aortic
cular channels within the embryonic disc that arches, similar to the corresponding fifth
coalesce into blood vessels. A pair of longitu- branchial arches, are rudimentary or nonexis-
dinally directed channels arise in a paramed- tent in humans. The sixth aortic arches contrib-
ian location to ultimately become the dor- ute to the pulmonary arteries and truncus arte-
sal aortae.3 riosus.l
From 21 to 25 days, the heart tubes fuse into The carotid system develops as a result of
a primitive heart, and the ventral aortic sac regression of three separate arterial segments.
becomes connected to the dorsal aortae by the Before involution of the first two aortic arches,
paired first aortic arches. By 32 days, six pairs blood flows to the cranial region from the ven-
of aortic arches have formed, coursing around tral aortic sac to the dorsal aorta through the
the five branchial arches. The first three arches first arches. However, by 29 days the first and
THE CAROTID ARTERY 791
between the internal carotid and primitive ments give similar results, and demonstrate a
neural arteries include the first cervical inter- gradual increase in size with age.a2
segmental, hypoglossal, and otic arteries. At the base of the neck, the common carotid
These arteries supplement the trigeminal and is deep to the sternomastoid, sternohyoid, and
are transiently present be tw een 24 and 29 day s. sternothyroid muscles and anterior to the
At29 days, the caudal branch of the internal fourth through sixth cervical transverse pro-
carotid forms the posterior communicating ar- cesses. The artery becomes more superficial at
tery. The posterior communicating artery the level of the cricoid cartilage, where it
quickly becomes the main blood supply of the crosses posterolateral to the intermediate ten-
rhombencephalon, and the trigeminal artery don of the omohyoid muscle to enter the ca-
recedes between 29 and 32 days. Between 32 rotid triangle (Fig. a).
and 35 days, the vertebral arteries form from The carotid triangle is in the infrahyoid por-
the anastomoses between cervical interseg- tion of the anterior triangle of the neck and is
mental arteries and join with the proximal end bounded anteroinferiorly by the superior belly
of the basiIar.28,a1 of the omohyoid, posteriorly by the sternoclei-
domastoid, and superiorly by posterior belly
of the digastric muscle. The carotid sheath lies
in the posterolateral aspect of the carotid trian-
NORMAL ANATOMY gle. Within the carotid sheath the common ca-
rotid artery is medial to the internal jugular
The asymmetric fate of the embryologic vein and anteromedial to the vagus nerve. The
fourth arches leads to asymmetry of the defin- cervical sympathetic chain is embedded on the
itive carotid origins. The right common carotid
is one of the terminal branches the brachio-
cephalic (innominate) artery, arising at the
base of the neck posterior to the right sternocla-
vicular joint. The left common carotid is the
second branch of the aortic arch, arising at the
highest part of the aortic arch, posterolateral
to the brachiocephalic trunk. From its origin
in the superior mediastinum, the left common
carotid ascends anterior then anterolateral to
the trachea to enter the neck behind the left
sternoclavicular joint.
Variations in position of the carotid origins
are usually related to variations of aortic arch
anatomy. The most common variant is a com-
mon origin of the brachiocephalic and left com-
mon carotid arteries. This variant, the so-called
bovine arch, occurs in 7"/" to 27'/" of patients.2r
In 2.5"/" of patients, the right common carotid
arises directly from the arch. This is usually
associated with an aberrant right subclavian
artery arising distally from the arch, with the
right carotid as the first branch off the arch. In '
,i '1,, r,,
, /,,t,E \\ \\
7.2o/,, of patients, there is a common origin of |I
)1
7l,r n1,
posteromedial wall of the sheath.36 Above the be part of the aging process, evaluation of pa-
bifurcation, the internal carotid remains in the tients fewer than 50 years of age reveals tortu-
carotid sheath and retains the same relation- osity or coiling in up to 27"k of patients, and
ship to the internal jugular vein and vagus kinking in 3.57n.5'18
nerve. The position of the carotid bifurcation re-
At approximately the superior border of the flects the degree of embryologic migration of
thyroid cartilage, each common carotid bifur- the external carotid artery and is, therefore,
cates into internal and external branches. The variable. Angiographic studies report the level
carotid bulb, or sinus, represents the fusiform of the bifurcation with respect to the cervical
dilatation at the carotid bifurcation encom- vertebrae. Huber reports the bifurcation at C4
passing the proximal internal carotid and dis- to C5 in 48"/" of 658 bifurcations, and at C3
tal common carotid and is present in 40"/" of to C4 in 34"/".12 There are reported cases of
cases.2r From the bifurcation, the internal ca- bifurcation of the carotid in the thorax down
rotid usually projects posterolateral to the ex- to the T3 level,ao and the bifurcation can occur
ternal carotid. The artery then ascends medial as high as C2.In children the bifurcation is
to the posterior belly of the digastric muscle slightly higher, seen at C2 to C3 in 40% and
and leaves the carotid triangle. Above the pos- at C3 to C4 in 40%.18 The level of the bifurcation
terior belly of the digastric, the artery lies deep is symmetric in28"/" and is within one vertebral
in the suprahyoid carotid space, immediately segment from side to side in 65"h of patients.35
posterior and lateral to the parapharyngeal Other variations in the cervical carotids in-
space.ro clude external carotid branches off the com-
Near the skull base, the internal carotid is mon or internal carotid, aplasia of the internal
anterior and medial to the internal jugular carotid, and separate origins of the internal
vein. The ninth, tenth, and eleventh cranial and external carotids.lE
nerves and the superior cervical ganglion of At the authors' institution, an increasing
the sympathetic trunk are posterior to the ar- number of patients are undergoing carotid
tery. The twelfth nerve lies posterior and me- endarterectomy without prior conventional
dial, then crosses the artery in the carotid trian- angiography. To assist preoperative localiza-
gle. The carotid enters the petrous carotid tion of the carotid bifurcation, the authors have
canal and ascends for 1 cm before turning ante- begun filming cervical magnetic resonance
rior and medial within the petrous bone. Proxi- (MR) angiography studies with annotation ref-
mally, the horizontal segment is anterior and erencing the slice level to the cervical spine
medial to the middle ear cavity. At the foramen scout localizer. Using this MR angiography
lacerum the vessel turns superiorly to emerge technique, the authors reviewed the level of
from the carotid canal. The artery then runs bifurcation in 237 carotid arteries. The mean
anteriorly and medially, lateral to the sella tur- overall cervical level was C4-f 1.5 vertebral
cica, into the cavernous sinus. It then turns bodies (95% confidence)with a range from C2
upward and medial to the anterior clinoid pro- to C3 to C6 to C7. Patients fewer than 30 years
cess and pierces the dura to enter the subarach- of age had slightly higher bifurcations (C3-4
noid space. level), which was not statistically significant.
Within the cavernous sinus, the abducens Variations in the orientation of the carotid
nerve lies on the inferolateral aspect of the bifurcation also have been described. In about
internal carotid. The oculomotor and trochlear 80% of patients, the internal carotid arises pos-
nerves and the ophthalmic and maxillary divi- terior or posterolateral to the external carotid.
sions of the trigeminal nerve lie along the lat- In an evaluation of 587 angiograms, Tea137
eral wall of the sinus. found that in 4"/" the internal carotid is medial,
There is considerable variation in the course and in 8% the internal carotid is posteromedial.
and position of the common carotids and ca- Smith and Larsen reported that in 100 angio-
rotid bifurcations. Elongation of the common grams, the internal carotid artery arises pos-
and internal carotid arteries leads to tortuosity terolateral to the extension of the common ca-
and kinking. Angiographic studies have re- rotid artery axis in 38%, posterior in 507,, and
vealed tortuosity in 10% to 43"/" and a kink posteromedial in 87o.3s Trigaux and cowork-
rn 4"/o to 16%. Ischemic symptoms caused by ers38 evaluated 200 arteries at angiography and
kinking of the carotid have been reported but found that the internal carotid lies posterolat-
are uncommon.s Although often believed to eral to the external carotid in 48"/", posterior
794 DUNGAN & HEISERMAN
in 3 4o/o, and posteromedial in 73"/,. Knowled ge cervical internal carotid arteries in 25'/r. The
of these variations is not only important for difference could be explained by hypoplasia
angiographers but necessary for appropriate of the anterior cerebral ipsilateral to the
interpretation of carotid ultrasonography. smaller carotid.lT
The size and appearance of the carotid sinus The wall thickness of the normal carotid ar-
is highly variable. The maximal diameter of tery has been evaluated using Doppler tech-
the sinus averages 9.3 mm with a standard niques and is interesting in evaluating athero-
deviation of 1.6 mm.e The caliber of the cervical sclerotic plaque morphology. The wall of the
internal carotid arteries is usually symmetric, common carotid artery measures approxi-
and averages approximately 6.3 mm at the mately 0.7 rnrn, about 10% of the vessel lumen
midcervical level.e The size of the distal cervi- diameter.2s The geometry of the carotid bifur-
cal segment of the vessel is constant or de- cation has been studied to evaluate normal
creases slightly near the skull base.q'11 In a ranges for flow models. In a series of 35 angio-
study using carotid ultrasonography in 32nor- grams of essentially normal carotid bifurca-
mal volunteers aged 13 months to 79 years, no tions, the bifurcation angle between the inter-
significant difference in the internal diameter nal and external carotid artery was 53o with a
of the common carotid arteries was found.22 standard deviation of 20o.e Because of the many
Individual patients, however, may display sources of variation in the morphology of the
asymmetry in carotid caliber. Angiographic carotid bifurcation, this segment of the vessel
evaluation of 142 patients demonstrated has a highly variable appearance on carotid
greater than 5% difference in caliber of the angiograms (Fig. 5).
t
ts
$
STF
Figure 5. Lateral angiograms of eight carotid bifurcations. Variability in the appearance of the bifurcation
and carotid sinus is caused by both variations in the angle and sizes of the vascular lumens as well
as projection effects associated with the variable orientation of the bifurcation in the neck.
THE CAROTID ARTERY 795
sured velocities in the internal carotid increase stenosis using angiography or MR angiogra-
in the presence of stenosis, and this forms the phy. Cross-sectional area measurements
basis of noninvasive e\.aluation of carotid ste- throughout the cardiac cycle should also be
nosis by Doppler ultrasonography. possible using gradient echo recalled MR im-
Volume flow information can be obtained aging, which could demonstrate nonconcen-
from Doppler and B-mode ultrasound mea, tric size changes, as seen in the aorta.6
surements2s; however, the approach requires Flow in the region of the carotid artery bifur-
detailed knowledge of the velocity profile cation reflects the complex vessel anatomy in
within the vessel and this limits the accuracy of this segment. The carina of the bifurcation acts
the method. Cine-phase contrast MR scanning as a flow divider, with approximately two
provides a direct measurement of volume flow thirds of the flow entering the internal carotid
throughout the cardiac cycle (Fig. 7), and can artery. Fluid velocities in the proximal internal
thus evaluate per cycle or per minute flow carotid artery tend to be greatest along the
rates in the carotid artery, which are approxi- wall adjacent to the bifurcation. Flow adjacent
mately 300 mllmin at rest.7 to the opposite wall of the carotid sinus is
Flow within the carotid artery is driven by characterized by recirculation in young indi-
the blood pressure. The putse'pressure, th"e viduals, documented by carotid ultrasonogra-
difference between the systolic and diastolic phy. Flow reversal occupies about one third
pressures/ averages 50+9 mm Hg in young of the carotid sinus, beginning at early or peak
populations and increases slightly in older systole and persisting for about 20"/" of the
populations. Because of blood vessel elasticity, cardiac cycle. Blood in this portion of the bulb
there is a slight increase in the diameter of is stagnant in diastole.2e,20 Diastolic acquisition
the carotid artery in systole compared with of MR angiography data is a strategy that takes
diastole, measurable by ultrasound. In young advantage of this fact to minimize intravoxel
populations, the increase at the level of the dephasing in the region of a stenosis.32 Similar
common carotid artery is about 10%, with a patterns of flow have also been documented
steady decrease to about 6% in older poputa- in fixed cadaver carotid bifurcations under
tions.3o Similar values are observed af thb ca- conditions of steady flow (Fig. B).23 This distri-
rotid bulb.2e This variation could lead to vari- bution of velocities results in high shear
ability in measurements of percent carotid stresses along the wall adjacent to the bifurca-
400
300
.s
C
: 200
E
100
20 40 on 100
% Cardiac Cycle
Figure 7. Variation of flow within the internal carotid artery throughout the cardiac
cycle determined by phase contrast cine MR. Flow is antegrade throughout the
cardiac cycle in this low-resistance circuit. (Adapted from Enzmann DR, Ross MR,
Marks MP, et al: Blood flow in major cerebral arteries measured by phase contrast
cine MR. AJNR 15: 123-129, 1994 @ by American Society of Neuroradiology;
with permission.)
THE CAROTID ARTERY 797
carotid artery can result in a superimposed 5. Busuttil RW, Memsic L, Thomas DS: Coiling and kink-
helical flow pattern in the internal carotid ar- ing of the carotid artery. In Rutherford RB (ed): Vascu-
lar Surgery, ed 4. Philadelphia, WB Saunders, 1995
tery.r6 Secondary flow in a curved vessel can 6. Chien D, Saloner D, Laub G, et al: High resolution
be a source of signal loss in magnetic resonance cine MRI of vessel distention. J Comput Assist Tomogr
angiography.33 These conditions apply to the 78:576-580,1991
carotid artery at the skull base, where multiple 7. Enzrnann DR" Ross MR, Marks MP, et al: Blood flow
bends result in helical flow patterns, as has in major cerebral arteries measured by phase contrast
cine MR. AJNR Am J Neuroradiol 15:723-129,7994
been demonstrated in models and simula- B. Fishman AP, Richards DW. The cerebral circulation.
tions.la }t Circulation of the Blood: Men and Ideas. New York,
Focal areas of vascular narrowing have little Oxford University Press, 7964, pp 703
effect on total flow in a vessel until a critical 9. Forster FK, Chikos PM, Frazier JS: Geometric model-
stenosis is reached. Beyond this value, gener- ing of the carotid bifurcation in humans: Implications
in ultrasonic Doppler and radiologic investigations.
ally about a 70/" reduction in area or a 50'/" J Clin Ultrasound 13:385-390, 1985
reduction in diameter, flow rapidly decreases 10. Gabella G: Cardiovascular anatomy. In Bannister LH,
as the pressure drop across the stenosis in- Berry MM, Collins P, et al (eds): Gray's Anatomy, ed
creases.' 38. New York, Churchill Livingstone, 1995, p 1,45
11. Gabrielson TO, Greitz T: Normal size of the internal
carotid, middle cerebral and anterior cerebral arteries.
Acta Radiol Diagn 10:1-10, 1970
CONCLUSION 12. Huber P: Cerebral Angiography, ed 2. New York,
Thieme Medical Publishers, 1982
Advances in the imaging evaluation of the 13. Kaplan HA, Ford DH: The Brain Vascular System.
carotid artery have contributed to a more com- Amsterdam, Elsevier, 1965
14. Kerber CW, Heilman CB: Flow dynamics in the human
plete understanding of the normal anatomy
carotid artery: I. Preliminary observations using a
and physiology of this important vessel. This transparent elastic model. AJNR Am ] Neuroradiol
improved understanding has pointed the way 13:173-180,1992
to a more accurate and less invasive evaluation 15. Kerber CW, Liepsch D: Flow dynamics for radiologists
of carotid artery disease (Table 1). I. Basic principles of fluid flow. AJNR Am J Neurora-
diol 15:1065-1075, 7994
16. Kerber CW, Liepsch D: Flow dynamics for radiologists
II. Practical considerations in the lir.e human. AJNR
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THE CAROTID ARTERY 799
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