Journal of Cranio-Maxillo-Facial Surgery 44 (2016) 734e742

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Journal of Cranio-Maxillo-Facial Surgery

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Three-dimensional computed tomographic analysis of variations

of the carotid artery*
Tetsuji Nagata*, Kazuma Masumoto, Yutaro Hayashi, Yoshiko Watanabe, Yuta Kato,
Fuminori Katou
Department of Dentistry and Oral and Maxillofacial Surgery, Hamamatsu University School of Medicine, Hamamatsu, Shizuoka, Japan

a r t i c l e i n f o a b s t r a c t

Article history: Background: Although the terms tortuous, coiling, and kinking have been used to describe the curvature
Paper received 25 December 2015 of the carotid artery, the prevalence rates of these patterns have differed among studies. We morpho-
Accepted 22 February 2016 logically evaluated the characteristics of the carotid artery by means of three-dimensional computed
Available online 2 March 2016
tomography (3DCT) to clarify the prevalence of tortuosity, coiling, and kinking. We present our results
and discuss the clinical impact of our findings.
Keywords:
Methods: A total 148 patients underwent contrast-enhanced CT (including 55 patients who underwent
Carotid artery
dynamic CT), and anatomical variations were analyzed on the basis of 3DCT images.
Three-dimensional computed tomography
Neck dissection
Results: Among the 296 arteries, tortuosity was present in 254 (85.8%), coiling in 9 (3.0%), kinking in 3
(1.0%), and occlusion in 2 (0.7%).
Conclusion: 3DCT image reconstruction is an effective means for classifying morphological variations of
the ICA and detecting abnormalities of the carotid artery. It can thereby potentially reduce the risk of
serious complications during neck surgery.
© 2016 Published by Elsevier Ltd on behalf of European Association for Cranio-Maxillo-Facial Surgery.

1. Introduction et al., 2003; Sacco et al., 2007). Recent advances in multidetector-

The internal carotid artery (ICA) runs along the neck lengthwise,
but is often tortuous. Tortuosity of the carotid artery is clinically
important because it has been linked to cerebrovascular disease,
including carotid artery stenosis, transient ischemia, and stroke
(Leipzig and Dohrmann, 1986; Koskas et al., 1993; Phan et al., 2012).
In addition, a tortuous carotid artery is associated with a risk of fatal
bleeding in peritonsillar surgical operations (tonsillectomy and
tonsillar abscess incision), requiring caution by otolaryngologists
(Corso et al., 1998; Ozcan et al., 2008; Hosokawa and Mineta, 2009;
Ogul et al., 2015). Such deformities of the carotid artery have been
demonstrated in angiographic, ultrasonographic, magnetic reso-
nance imaging (MRI), and cadaver studies (Metz et al., 1961; Weibel
and Fields, 1965; Pancera et al., 2000; Paulsen et al., 2000; Oliviero
*
This study was supported in part by a Grant-in-Aid for Scientific Research from
the Ministry of Education, Culture, Sports, Science and Technology, Japan (No.
25460680).
* Corresponding author. Department of Dentistry and Oral and Maxillofacial
Surgery, Hamamatsu University School of Medicine, 1-20-1 Handa-yama, Higashi-
ku, Hamamatsu City, Shizuoka 431-3125, Japan. Tel./fax: þ81 53 435 2349.
E-mail address: nagatez@hama-med.ac.jp (T. Nagata).
row computed tomography (CT) and imaging techniques using
volume-rendering reconstruction software have allowed recon-
struction of three-dimensional images, enabling more precise
analysis (Sakaguchi et al., 2014). We morphologically evaluated the
characteristics of the carotid artery by means of three-dimensional
CT (3DCT) to clarify the prevalences of tortuosity, coiling, and
kinking. We present our results and discuss the clinical impact of
our findings.
2. Material and methods
From January 4, 2012, through August 10, 2015, enhanced CT
was performed in 150 patients who were treated in the Department
of Oral and Maxillofacial Surgery, Hamamatsu University Hospital.
Two patients were excluded because of poor image quality caused
by artifacts. The remaining 148 patients (86 males and 62 females;
median age, 63.9 years; range 13e88) were studied. The patients
had 133 oral cancers, 6 maxillofacial injuries, 5 benign tumors, and
4 severe maxillofacial infections. The mean age of the patients was
relatively high because many had oral cancer, which typically af-
fects older persons. Of the 148 patients, 55 underwent dynamic CT
in preparation for superselective chemotherapy and microsurgery.

http://dx.doi.org/10.1016/j.jcms.2016.02.011
1010-5182/© 2016 Published by Elsevier Ltd on behalf of European Association for Cranio-Maxillo-Facial Surgery.
 T. Nagata et al. / Journal of Cranio-Maxillo-Facial Surgery 44 (2016) 734e742
CT images were obtained using an Aquilion MULTI 64-MDCT
scanner (Toshiba Medical Systems, Tokyo, Japan) and a SOMA-
TOM Definition Flash (Siemens AG, Munich, Germany). The effec-
tive dose to the whole body evaluated according to International
Commission on Radiologic Protection (ICRP) publication 103 when
CT scanning is performed from the skull base to the aorta with these
2 scanners was estimated to be 7.76 mSv and 4.38 mSv, respectively
(ICRP, 2007; Takahashi et al., 2015). A non-ionic agent, Omnipaque
(Daiichi Pharmaceutical, Tokyo, Japan), was used as the contrast
medium. The volume data were transferred to a workstation, and
Synapse Vincent software (FUJIFILM, Tokyo, Japan) was used to
conduct image analysis. The 3D reconstruction of the carotid artery
was performed using this software to create 3D images from two-
dimensional (2D) images. The jugular vein, maxilla, and mandible
were removed from the images as required to facilitate 3D exam-
ination of the carotid artery.
2.1. Morphological variations
2.1.1. Morphological classification
The morphological classification used in this study was a
modified version of the criteria proposed by Weibel and Fields
(1965). Because there is no clear distinction between normal and
tortuous in their original classification, we added Paulsen's criteria
to facilitate objective evaluation (Paulsen et al., 2000) (Fig. 1). Our
classification was as follows: straight: the internal carotid artery
(ICA) angle was less than 15 and the course of the ICA was straight;
tortuous: the ICA angle was not less than 15 or the course of the
ICA was S- or C-shaped; coiling: an exaggerated S-shaped curve or a
circular configuration; and kinking, angulation of 1 or 2 or more
segments associated with stenosis.
2.1.2. Carotid bifurcation angle
The ICA angle was defined as the angle between the common
carotid artery and the ICA centerlines in the 3D space (Fig. 1). This
angle was measured on the 3D images.
2.1.3. Tortuosity index
To assess the degree of tortuosity of the carotid artery, the tor-
tuosity index (TI) was calculated. The vessel length of the carotid
artery (VLCA) is the distance from its origin to the skull base along
the arterial centerline. Because the origins differ between the right
and left common carotid arteries, the measurement points differed
on the right and left: the right origin of the carotid artery is the
brachiocephalic trunk, and the left origin is the aortic arch. The
distance of the carotid artery (DCA) was defined as the shortest
distance between the same points on the 3D image. TI was calcu-
lated as TI ¼ VLCA/DCA (Fig. 2).
2.2. Variation of course
2.2.1. Criteria for posterior deviation
To assess posterior deviation (PD) of the carotid artery, a
transverse process line (TPL) connecting 5 processes of the cervical
vertebrae (C1eC5) on a lateral view was drawn. If a carotid artery
with ventrodorsal curvature ran beyond the TPL on 3DCT images, it
was judged to be PD positive (Fig. 3).
2.2.2. Relation to pharyngeal wall
To assess the relation to the pharyngeal wall or tonsillar bed, the
superior and medial deviation were examined. If deviation to
pharyngeal posterior wall was observed, it was classified as
positive.
735
3. Results
3.1. Morphology of the carotid artery
Of 296 arteries, tortuosity was present in 254 arteries (85.8%),
coiling in 9 (3.0%), kinking in 3 (1.0%), and occlusion in 2 (0.7%).
Tortuosity and coiling were found at nearly the same frequencies
on the left and right sides. Kinking was more frequent on the left
side than on the right side. Occlusion was found in only 2 patients,
both on the right side (Table 1). The prevalence of variations in
carotid artery morphology and the ICA angle increased in patients
50 years or older (Table 2, Fig. 4). A scattergram of the relation
between age and TI indicated a slightly strong correlation (Pearson
product e moment correlation coefficient, r ¼ 0.69616) (Fig. 5).
VLCA gradually increased with age on both sides, whereas DCA
decreased in patients 60 years or older (Fig. 6).
3.2. Course of the carotid artery
Posterior deviation of the carotid artery was noted in 72 of the
tortuous arteries and 2 of the kinking arteries (total 25.0%). Those
posterior deviated carotid arteries form an omega-shaped loop.
Deviation to pharyngeal wall was noted in 7 arteries, 4 of which
were located on the right side (Table 1).
3.3. Typical presentations
3.3.1. Straight ICA
Straight ICAs were found in a 13-year-old girl with a benign
tumor of the mandible. 3DCT showed that both carotid arteries
were straight, with no posterior deviation. The right ICA angle was
11.4 , and the left ICA angle was 12.1. The right TI was 1.02, and the
left TI was 1.01 (Fig. 7).
3.3.2. Tortuous ICA
Tortuous ICAs were found in a 79-year-old man with carcinoma
of the tongue. 3DCT showed tortuosity of both carotid arteries,
accompanied by posterior deviation. Moreover, the right common
carotid artery meandered in the lower neck. The right ICA angle
was 31.5 , and the left ICA angle was 56.4 . The right TI was 1.29,
and the left TI was 1.24 (Fig. 8).
3.3.3. Coiling ICA
Coiling ICAs were seen in a 77-year-old man with carcinoma of
the tongue. 3DCT imaging demonstrated coiling of the right carotid
artery and tortuosity of the left carotid artery, without posterior
deviation. The right ICA formed a loop at the level of the naso-
pharynx. The right ICA angle was 28.1, and the left ICA angle was
24.4 . The right TI was 1.37, and the left TI was 1.23 (Fig. 9).
3.3.4. Kinking of the ICA
Kinking of the ICA was found in a 78-year-old woman with car-
cinoma of the lower gum. 3DCT imaging showed tortuosity of the
right carotid artery, with low bifurcation and kinking of the left ca-
rotid artery with posterior deviation. The kinking was apparent, but
there was no occlusion. The right ICA angle was 19.2 , and the left ICA
angle was 48.2 . The right TI was 1.20, and the left TI was 1.42 (Fig. 10).
3.3.5. Deviation to the posterior wall of the pharynx
Deviation of the ICA towards the posterior wall of the pharynx
was seen in a 62-year-man who had carcinoma of the tongue. 3DCT
and axial CT imaging revealed a tortuous right ICA drawing an arc
toward the posterior wall of the pharynx. The patient had no sense
of incongruity in the pharynx. The right ICA angle was 25.8 , and
736 T. Nagata et al. / Journal of Cranio-Maxillo-Facial Surgery 44 (2016) 734e742

Fig. 1. Schematic drawing of morphological classification of carotid artery, viewed from the right lateral side. ICA, internal carotid artery; ECA, external carotid artery. #, internal
carotid artery angle.

Fig. 2. 3DCT images of the carotid artery on both sides. Measurement of the shortest distance of the carotid artery (DCA) and the vessel length of the carotid artery (VLCA) are
shown. Because the origins of the common carotid arteries differ between the right and left sides, the point of measurement is different on each side. DCA, measured from the aortic
arch or the right subclavian artery to the carotid canal (arrow) in the temporal bone, is indicated by the orange dotted line, and VLCA is indicated by the red line. (a) Right side view.
(b) Left side view.

the left ICA angle was 47.4 . The right TI was 1.21, and the left TI was center points of the carotid artery in the axial CT images were
1.15 (Fig. 11). identified manually, drawing of the vascular centerline required a
The lengths and angles mentioned above were measured on 3D little time. Consequently, about 30 min per case were required to
images with the use of SYNAPSE VINCENT software. Because the prepare the detailed images and measure all specified variables.
 T. Nagata et al. / Journal of Cranio-Maxillo-Facial Surgery 44 (2016) 734e742 737

Fig. 3. Schematic drawing of posterior deviation viewed from the right lateral side. Transverse process line of the cervical vertebrae C1eC5 is indicated by the red dotted line. (a)
Posterior deviation negative. (b) Posterior deviation positive. Black star: transverse process of atlas; filled circle: transverse process of the cervical vertebrae C2eC5.

Table 1
Prevalence of the carotid artery (CA) classification for 296 CA.

Straight Tortuosity Coiling Kinking Occlusion Total

Right CA 14 127 (32) [4] 5 0 2 148

Left CA 14 127 (40) [3] 4 3 (2) 0 148
Total 28 254 (72) [7] 9 3 (2) 2 296
(%) 9.5 85.8 3.0 1.0 0.7

Data in parentheses are posterior deviation beyond the transverse process line
C1eC4.
Data in square brackets are deviation to the pharyngeal wall.

Table 2
Prevalence of the carotid artery (CA) classification according to age.

Age Straight Tortuosity Coiling Kinking Occlusion Total

10e19 2 2 0 0 0 4
20e29 4 2 0 0 0 6 Fig. 4. ICA angle according to age. ICA, internal carotid artery.
30e39 5 17 0 0 0 22
40e49 5 7 (6) 0 0 0 12
50e59 5 50 (12) 0 0 1 56
60e69 2 71 (18) [3] 1 0 0 74
70e79 4 60 (21) [3] 4 (1) 3 (1) 1 72
80e89 1 45 (17) [1] 4 0 0 50
Total 28 254 9 3 2 296

Data in parentheses are posterior deviation beyond the transverse process line
C1eC4.
Data in square brackets are deviation to the pharyngeal wall.

4. Discussion

Morphological anomalies of the internal carotid arteries of the

neck are a known phenomenon. Previous studies have reported
that the prevalence of morphological variations ranges from 4% to
66% (Metz et al., 1961; Leipzig and Dohrmann, 1986; Macchi et al.,
1997; Pancera et al., 2000; Paulsen et al., 2000). These estimates are
based on the results of arteriographic, ultrasound, contrast- Fig. 5. Scattergram of the relation between age and tortuosity index (TI), indicating a
enhanced CT, MRI, and cadaver studies. Differences in prevalence slightly strong correlation.
738 T. Nagata et al. / Journal of Cranio-Maxillo-Facial Surgery 44 (2016) 734e742
Fig. 6. VLCA and DCA according to age. VLCA, vessel length of the carotid artery; DCA,
distance of the carotid artery.
Fig. 7. Straight carotid artery in a 13-year-old girl. 3DCT image of the neck after the jugular vein, maxilla, and mandible have been removed by software. The carotid artery is
straight, and an intervertebral space is evident. (a) Right side view. (b) Frontal view. (c) Left side view.
rates may be attributed to differences in diagnostic techniques, the
selection criteria used to define the study population, and the
classifications used to define vascular anomalies (Sacco et al.,
2007).
In the present study, 3DCT images were created with the use of
image analyzing software, SYNAPSE VINCENT. By using this soft-
ware, 3D images can be easily obtained, without technical knowl-
edge of programming. As compared with MRI, CT imaging has the
advantage of precisely depicting hard tissue. This method therefore
can provide not only objective detailed information on the struc-
ture of the carotid artery, such as the bifurcation angle and vessel
length, but also on the anatomic relation between the carotid artery
and cervical vertebrae. In this respect, CT imaging is considered
superior to MRI.
The results of our morphological analysis indicated that tortu-
osity was present in 254 arteries (85.8%), coiling in 9 arteries (3.0%),
kinking in 3 arteries (1.0%), and occlusion in 2 arteries (0.7%).
Weibel and Fields reported that the prevalence of tortuosity, coil-
ing, and kinking ranged from 10% to 44%, 0.4% to 4%, and 3% to 15%,
respectively (Weibel and Fields, 1965). Paulsen studied the course
of the carotid artery in specimens obtained from 282 cadavers and
reported that the course was straight in 67.8% of the specimens,
curved in 26.2%, and kinking or coiling in 6% (Paulsen et al., 2000).
The higher prevalence of variations in our study than in previous
studies is most likely attributed to the high mean age of the pa-
tients, the criteria used to define the ICA angle (straight: less than
15 ), and genetic differences among the study populations. How-
ever, our finding that the prevalence of anomalies of the carotid
artery increased with advancing age is in accord with the results of
other studies.
Abnormalities of the carotid artery can result from congenital
deformity as well as acquired changes (Ricciardelli et al., 1989).
Because carotid artery tortuosity is found in children, this anomaly
is thought to be of congenital origin (Xu and Uwiera, 2010). How-
ever, most cases of tortuosity are found in elderly individuals, and
the prevalence increases with age. Therefore, peripheral vascular
abnormalities caused by hypertension, hyperlipidemia, athero-
sclerosis, and smoking are thought to contribute to acquired carotid
artery tortuosity (Barbera et al., 2006). Jackson et al. clinically and
experimentally showed that substantial axial strain was necessary
to sustain the morphological stability of arteries and that a reduc-
tion in strain resulted in arterial tortuosity (Jackson et al., 2005).
Thus, loss of elasticity with aging causes vessel elongation, leading
to the development of tortuosity (Chilvers et al., 1974; Wensing
 T. Nagata et al. / Journal of Cranio-Maxillo-Facial Surgery 44 (2016) 734e742 739

Fig. 8. Tortuosity of the carotid artery in a 79-year-old man. The ICA bilaterally runs beyond the transverse process line and curves at the caudalis of the transverse process of the
atlas (arrow), forming an omega-shaped loop. (a) Right side view. (b) Left side view.

Fig. 9. Coiling of the carotid artery in a 77-year-old man. The right carotid artery coiled (arrow), forming a loop at the level of the nasopharynx. (a) Right side view. (b) Frontal view.

et al., 1995; Barbera et al., 2006; Kamenskiy et al., 2015). On the
other hand, a decrease in anatomical distance may also contribute
to such tortuosity. Tsunoda et al. reported that advanced age with a
bent posture (cervical kyphosis) shortens the distance between the
central carotid artery and the skull base, and thus increases the
incidence of aberrations of the internal and common carotid
arteries (Tsunoda et al., 2005). It is known that degenerative
changes of the cervical spine, such as decreased height of the
vertebral body and disc with advancing age, result in shortening of
the neck (Yukawa et al., 2012). Our study demonstrated that DCA
decreased with age, whereas VLCA increased with age. When
elderly patients were compared with young patients, a decrease in
740 T. Nagata et al. / Journal of Cranio-Maxillo-Facial Surgery 44 (2016) 734e742

Fig. 10. Kinking of the carotid artery in a 78-year-old woman. The left carotid artery showed kinking (arrow) with posterior deviation. The kinking was apparent, but did not occlude
the artery. (a) Frontal view. (b) Left side view.

Fig. 11. Deviation of the internal carotid artery towards the posterior wall of the pharynx in a 62-year-old man. 3DCT and axial CT imaging revealed a tortuous right internal carotid
artery drawing an arc towards the posterior pharynx (arrow). (a) Right side view. (b) Frontal view. (c) Axial image.

intervertebral disk height was evident on 3DCT. Moreover, Hoso-
kawa et al. reported that a “lifted-up aorta” at right angles toward
the head, which resulted from hypertrophy of the heart, induced
tortuosity of the ICA (Hosokawa and Mineta, 2009). These findings
indicate that tortuosity is accelerated not only by loss of elasticity,
but also by shortening of the distance of the vessel due to aging. Our
results indicate that both VLCA and DCA differ considerably among
individuals. Continuous follow-up of individual changes is thus
needed in the future.
Owing to vascular malformation, some arteries run an abnormal
course. Many reports have described an aberrant carotid artery
presenting with a pharyngeal mass or dysphagia (Choi et al., 1998;
Ozcan et al., 2008; Hosokawa and Mineta, 2009; Xu and Uwiera,
2010; Ogul et al., 2015). The prevalence of the ICA with deviation
to pharyngeal wall was 3.3% in our study, which is consistent with
the results of other studies, but none of our patients had symptoms
such as a sense of incongruity in the pharynx.
Posterior deviated carotid arteries form an omega-shaped loop,
and this is clinically a significant issue for a head and neck surgeon.
Neck dissection is the most effective and the most widely used
surgical procedure for the control of cervical lymph node metas-
tasis, and the ICA must be preserved. When a curved ICA is present
dorsally beyond the posterior process line, a loop of the artery is
recognized in the upper internal jugular region (level IIA) and
 T. Nagata et al. / Journal of Cranio-Maxillo-Facial Surgery 44 (2016) 734e742
Fig. 12. Intraoperative view of the left side neck in a 61-year-old woman. Functional
neck dissection with jugular vein resected (upper triangle) and accessory nerve
preservation (lower triangle) was performed. A posterior deviated internal carotid
artery formed a loop in an omega shape in the region of level II (arrow).
accessory nerve region (level IIB). The transverse process of atlas is
considered an anatomic landmark for the dissection because the
ICA, the internal jugular vein, and the spinal accessory nerve all sit
anterior to it (Sheen et al., 1997). An abnormal appearance (omega
shape) of the ICA in the accessory nerve region is not known;
however, a corrosion vascular cast model has been described for 1
patient (Paulsen et al., 2000). In this situation, the carotid artery is
at high-risk for injury during neck dissection, potentially leading to
the development of fatal complications (Fig. 12). Imaging evalua-
tions are routinely performed by CT, MRI, and positron emission
tomography before neck dissection, but it is easy to miss the high-
risk curvature of the ICA on these slice images. On the other hand,
3DCT, which allows the status of the carotid artery to be precisely
observed, was very effective for identifying variations in the carotid
artery. The prevalence of head and neck cancer is increasing among
elderly persons, and more elderly patients are hereafter expected to
undergo neck dissection. Head and neck surgeons should therefore
preoperatively confirm the features of the carotid arteries by 3DCT
imaging in individual patients.
3DCT image reconstruction does have several limitations. First,
creating detailed images and measuring the VLCA requires a
somewhat prolonged time (approximately 30 min per case) in this
analysis. Second, the effects of metallic dental artifacts interfere
with detailed analysis. Third, radiation exposure is inevitable.
However, given that 3DCTs were analyzed by using data obtained
from routine CT, and that the effect dose to the whole body was
4.38e7.76 mSv per scan, radiation exposure to the patients is
considered clinically minimal.
741
5. Conclusion
3DCT image reconstruction is an effective means for classifying
morphological variations of the ICA and detecting abnormalities of
the carotid artery, and can thereby potentially reduce the risk of
serious complications during neck surgery.
Conflict of interest statement
All authors declare that there is no conflict of interest.
Acknowledgments
We thank Medical Network K.K., Tokyo, Japan for help in writing
the manuscript in English. This study was supported in part by a
Grant-in-Aid for Scientific Research from the Ministry of Education,
Culture, Sports, Science and Technology, Japan (No. 25460680). No
benefits in any form have been or will be received from a com-
mercial party directly or indirectly related to the subject of this
manuscript.
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