Key-words: Carotid anatomy - carotid bifurcation level - carotid endarterectomy - computed tomographic
angiogram carotid study - extracranial carotid branching patterns
Introduction
The level of common carotid bifurcation and branching patterns of external carotid
arteries have significant impacts on various surgical procedures of the head-and-neck
region. In neurosurgery, the level of bifurcation impacts the decision-making in carotid
endarterectomy and stenting procedures for carotid stenosis. The endarterectomy should
be avoided in patients with very high carotid bifurcation, usually defined as being
above the C3 vertebral body. From the surgical perspective, high-level carotid bifurcation
requires more specialized techniques for adequate exposure and has more tendency to
postoperative complications because of difficulties in the dissection of distal carotid
artery and risk of injuries to adjacent structures, including hypoglossal nerve and
salivary gland.[[1 ]],[[2 ]],[[3 ]],[[4 ]] Variation of branching patterns of carotid arteries needed to be carefully evaluated
preoperatively and during the carotid endarterectomy procedure because these branches
needed to be cross-clamped to control bleeding.
Interestingly, even in the era of modern imaging techniques, most of the studies about
the carotid bifurcation and the branching patterns were still performed in cadaveric
specimens.[[5 ]],[[6 ]],[[7 ]],[[8 ]],[[9 ]],[[10 ]],[[11 ]],[[12 ]],[[13 ]],[[14 ]],[[15 ]],[[16 ]] We believe that computed tomographic angiogram (CTA) of carotid can provide excellent
visualization of anatomical variations and can be applied in clinical practice comparable
to or even better than cadaveric data. Some studies used CTA or magnetic resonance
angiography (MRA) of carotid as a method to determine the level of the carotid bifurcation.[[17 ]],[[18 ]],[[19 ]] However, each study defined different landmarks for determining the level of bifurcation,
making the results from these studies incomparable. The aim of this study is to investigate
the variations of common carotid artery bifurcation comparing with the level of the
vertebral column and branching pattern of the external carotid artery using CTA with
three-dimensional (3D) reconstruction.
Methods
We reviewed the consecutive 100 patients with carotid CTAs from the PACS database
performed in Prasat Neurological Institute from January 2013 to May 2016.
Multisection CTAs were obtained with a 64-slice CT scanner (SOMATOM Definition AS,
Siemens Medical Systems Inc., Erlangen, Germany). Contrast media was injected at a
rate of 5 mL/s, with the use of a power injector (Mallinckrodt) and an 18G or 20G
needle inserted in the antecubital vein. The volume of iodinated contrast media in
each study was 100 ml. The CTA was automatically started with bolus trigger (Care-Bolus)
by monitoring of vascular opacification. The scanning parameters included 120 kV,
129 mAs, 0.6-mm slice thickness, 0.6 s scan time, 0.33 s rotation time, 1.4 pitch,
and 200 mm Field of View (FOV). Transverse spiral scan from vertex to the arch of
the aorta was performed for the entire carotid artery system. Postprocessing subtraction
image, volume rendering, and maximum intensity projection image were created on medical
workstations (Syngo Via and Syngo InSpace).
Levels of carotid bifurcation were compared relatively with the level of the vertebral
body and ipsilateral angle of the mandible in horizontal plane. Branching patterns
of carotid arteries including superior thyroid, facial, lingual, and occipital arteries
were examined from 3D imaging. Anterior branches were classified as A1, superior thyroid,
facial, and lingual arteries arose from separate branches of external carotid arteries;
A2, facial arteries arose in common trunk with lingual arteries (linguofacial trunk)
and A3, lingual arteries arose with superior thyroid arteries (thyrolingual trunk)
[[Figure 1 ]]. Occipital arteries branching patterns were classified as O1, occipital arteries
arose between superior thyroid arteries and lingual arteries; O2, occipital artery
arose between lingual arteries and facial arteries and O3, the occipital arose above
facial arteries [[Figure 2 ]].
Figure 1: The artistic rendering illustrates the classification of the anterior branch of the
external carotid artery into three common variations. A1: The superior thyroid, lingual,
and facial arteries arose from separate branches of the external carotid artery; A2:
The facial artery arose in common trunk with the lingual artery (linguofacial trunk);
and A3: The lingual artery arose in common trunk with superior thyroid artery (thyrolingual
trunk)
Figure 2: The artistic rendering illustrates the classification of the occipital artery into
three common variations. O1: The occipital artery arose between superior thyroid artery
and lingual artery; O2: The occipital artery arose between lingual artery and facial
artery; and O3: The occipital artery arose above the level of the facial artery
The data were descriptively analyzed and reported into frequency, median, and percentage.
The study was approved by the Prasat Neurological Institute Ethics Committee.
Results
Level of carotid bifurcation comparing with the vertebral column and angle of mandible
CTA of 200 carotid arteries from 100 patients were examined, 58% were men. The mean
age was 60-year-old (age range 19–91, median 62).
Sixty-one percent of CTA was performed for diagnosis and illustrated carotid anatomy
for patients with carotid stenosis. There is only one carotid artery that the level
of bifurcation cannot be identified from CTA due to nearly occluded ICA bifurcation.
The carotid bifurcation was most commonly located at C3–C4 vertebral level, followed
by mid C4, and mid C3, respectively [[Table 1 ]]. There was no significant difference between the two sides of carotid arteries.
Table 1: The distribution of level of carotid bifurcations comparing with the level of the
vertebral body
Comparing level of angle of mandible in neutral supine position with vertebral body
showed that the most common level of angle of mandible was at C2–C3 (51%), followed
by mid C3 (28%), mid C2 (13%), C3–C4 (5%), and C4–C5 (3%), respectively. We found
no angle of the mandible that located below C4–C5 level in our study [[Table 2 ]].
Table 2: The distribution of level of the angle of mandible comparing with the level of the
vertebral body
Most of the carotid bifurcations (83.5% of the total, 86% of the right side, 81% of
left side) were located below the angle of mandible, with a mean distance of 16.41
mm below the angle on the right side and 14.84 mm on the left side. Sixteen percent
of carotid bifurcation was lying above or at the same level of the angle of the mandible
[[Table 3 ]].
Table 3: The relationship of level of carotid bifurcation comparing with the level of the
angle of mandible
Branching patterns of superior thyroid, lingual, facial, and occipital arteries
From 200 carotid arteries, CTA studies with 3D reconstruction, we excluded five samples
of superior thyroid, facial, lingual arteries (anterior branches, classified as A1,
A2, and A3) and 4 of occipital arteries due to poor visualization of branching patterns.
The superior thyroid, facial, and lingual arteries arose from separate branches of
external carotid arteries in 67.7% of samples. Facial arteries arose in common trunk
with lingual arteries in 29.2%, and the lingual arteries arose with superior thyroid
arteries in 2% [[Table 4 ]] and [[Figure 1 ]], [[Figure 2 ]], [[Figure 3 ]], [[Figure 4 ]], [[Figure 5 ]].
Table 4: Branching patterns of external carotid artery
Figure 3: The left-sided three-dimensional computed tomographic angiogram of a 47-year-old
male with carotid stenosis illustrates the branching pattern of the external carotid
artery. The superior thyroid artery (arrow), lingual artery (arrowhead), and facial
artery (asterisk) arise from separate branches of the external carotid artery; (A1).
The occipital artery arises above the origin of the facial artery; (O3)
Figure 4: The left-sided three-dimensional computed tomographic angiogram of 53-year-old male
with carotid stenosis illustrates the level of carotid bifurcation at C3-C4 intervertebral
space level and branching pattern of the external carotid artery. The facial artery
arises in common trunk (arrow) with the lingual artery; (A2). The occipital artery
(asterisk) arises above the origin of facial artery (asterisk); (O3)
Figure 5: The right-sided three-dimensional computed tomographic angiogram of a 59-year-old
male with carotid stenosis illustrates the branching pattern of the external carotid
artery. The superior thyroid artery arises in common trunk (arrow) with lingual artery;
(A3). The occipital artery (asterisk) arises between the origin of lingual (arrow)
and facial artery (arrowhead); (O2)
The occipital arteries arose between superior thyroid arteries and lingual arteries
in 49.5%, between lingual arteries and facial arteries in 32.7% and above facial arteries
in 15.8%. There were 2% of occipital arteries that arose in common trunk with superior
thyroid, lingual, or facial arteries [[Table 4 ]] and [[Figure 1 ]], [[Figure 2 ]], [[Figure 3 ]], [[Figure 4 ]], [[Figure 5 ]].
Discussion
Evaluation of carotid bifurcation level in patients with carotid stenosis, planning
for endarterectomy, was usually performed by CTA, MRA, or even conventional angiography.
Most recommendations suggest that carotid bifurcation above C3 vertebral level was
considered high bifurcation. A study used distance from the mastoid process as a reference
to identify the high bifurcation.[[18 ]] Some studies used thyroid cartilage as anatomical landmark.[[5 ]],[[7 ]],[[8 ]],[[9 ]],[[15 ]],[[16 ]] The level of carotid bifurcation was considered as a high bifurcation when it was
located above the thyroid cartilage.
In this study, the carotid bifurcations can be identified in 95.5% of the samples
and the branching patterns of external carotid arteries can be clearly identified
with CTA with multiplanar reconstruction (MPR) and 3D reconstruction in 97.75% of
the study sample, suggesting that CTA is an effective and reliable modality to evaluate
the carotid artery anatomy in patients undergoing carotid endarterectomy.
We reviewed the studies describing the carotid bifurcation in the literature and anatomy
textbooks [[Table 5 ]]. Using the vertebral body level as the anatomical landmark, most of the classic
western anatomy textbooks described that carotid bifurcation was found most commonly
located at C3–C4 vertebral level.[[20 ]],[[22 ]],[[23 ]],[[24 ]],[[25 ]],[[26 ]] Clemente reported that only 5% of his samples had high carotid bifurcation.[[20 ]] An angiographic study in Turkey reported 2% of samples with high bifurcation.[[21 ]] Interestingly, studies in Asian cadavers showed different results.[[6 ]],[[11 ]],[[12 ]],[[13 ]],[[14 ]] Klosek and Rungruang studied the level of carotid bifurcation comparing with the
level of the vertebral body in 43 Thai cadavers. They reported that most of the carotid
bifurcation was at C3–C4 vertebral level. However, the carotid bifurcation could not
be identified in 13.6% of the cadaver. The authors discussed that very high position
of carotid bifurcation could explain the finding.[[12 ]] Chaijaroonkhanarak et al., also reported a study in 55 Thai cadavers. The right
carotid bifurcation was the most common at C2 level and left bifurcation was the most
common at C3 level, with 53.6% of their cadavers had high carotid bifurcation.[[13 ]] Hayashi et al. reported 49 Japanese cadaveric dissection and found that most of
the carotid bifurcation was at mid C3 vertebral body level with 20% considered to
have high carotid bifurcation. The authors concluded that the carotid bifurcation
of Japanese might be located higher than those of the European population.[[11 ]] Another Japanese study reported a high bifurcation in 31.2% of their cadavers.[[14 ]].
Table 5: The distribution of the level of carotid bifurcation among reported studies
Our study found that most of the carotid bifurcation was located at the level of C3–C4
vertebral body, with 12% with high carotid bifurcation. We realized that with limited
study population, 200 carotid studies in 100 patients, cannot make a conclusion that
the Asian population have more percentage of high carotid bifurcation than in the
Caucasian population. However, our data are concordant with other previous carotid
studies performed in the Asian population and should be a concern for a clinician
who deals with this group of patients.
As Chaijaroonkhanarak et al., reported that carotid bifurcation in their cadaveric
dissection study most commonly located at C2 vertebral body,[[13 ]] suggested that most of the carotid bifurcations of their cadaveric specimen were
considered to be high carotid bifurcations. However, that may result from the technique
of measurement and cadaveric preparation that may cause errors in the evaluation of
the actual level of the carotid bifurcation.
From our surgical experience, the relationship between the angle of the mandible and
carotid bifurcation also has an impact on surgical exposure. We observed that carotid
bifurcation located at the level of or above the level of the angle of mandible usually
had more exposure difficulties. Most of carotid bifurcations (86% on the right side
and 81% on the left side) were located below the level of the angle of the mandible
in the supine neck position, and 16% was located at the level of the angle of mandible
or above the level of the angle of mandible. Further study has to be performed to
identify the relationship between the angle of mandible with difficulties in surgical
exposure.
The distribution of branching patterns of carotid arteries in this study is quite
different from other studies [[Table 6 ]].[[5 ]],[[7 ]],[[10 ]],[[11 ]],[[15 ]],[[27 ]],[[28 ]] The percentage of facial arteries that arose in common trunk with lingual arteries
(linguofacial trunk) was more frequently found (29.2% vs. 0%–20%). The branching patterns
of the occipital artery had the same distribution as the previous study.[[11 ]].
Table 6: The distribution of external carotid artery branching patterns among reported studies
Limitations
This is a retrospective, anatomical study with no comparative data. We assumed that
patients underwent CTA was in the supine position, but in the real surgical procedures,
these patients would be operated in extended position of the neck, thus studying the
level of the angle of mandible from CTA might has limited benefit in surgical planning.
As mentioned in the previous study,[[29 ]] the vertebral level of structures in the neck depends in part on the curvature
of the cervical spine and choice of the reference plane. As our study measured all
structures in horizontal plane, the level retrieved might be different from other
studies using the axial plane.
We evaluate the carotid bifurcation level from CTA, which was an intraluminal study.
The bifurcation level cannot be identified in those vessels with severe carotid stenosis
or completely obliterated carotid arteries, and also in very small vessels that usually
cannot be identified in normal imaging, for example, the ascending pharyngeal artery.
Conclusions
Carotid bifurcation level and carotid branching patterns should be preoperatively
evaluated and should be meticulously identified intraoperatively before arteriotomy
was performed to achieve well-controlled hemostasis during the procedure. Carotid
bifurcations and the branching patterns of external carotid arteries can be clearly
identified with CTA with MPR and 3D reconstruction, suggesting that CTA is an effective
and reliable modality for preoperative evaluation of the carotid system in patients
undergoing carotid endarterectomy and other carotid procedures. Furthermore, CTA can
be used to identify the relationship of level of the angle of the mandible and the
level of the carotid bifurcation, which can be benefit in preoperative planning.
Most of the carotid bifurcation located at level of C3–C4 vertebral body, concordant
with previous carotid studies performed in the Asian population. Carotid bifurcations
of Asian tend to be located slightly higher than those of Caucasian studies.
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent forms.
In the form the patient(s) has/have given his/her/their consent for his/her/their
images and other clinical information to be reported in the journal. The patients
understand that their names and initials will not be published and due efforts will
be made to conceal their identity, but anonymity cannot be guaranteed.
