Aberrations of the Cervical Carotid Artery Which May Be Dangerous in Pharyngeal Surgery—A Computed Tomographic Study

doi:10.4236/act.2013.21006

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Advances in Computed Tomography, 2013, 2, 29-33

http://dx.doi.org/10.4236/act.2013.21006 Published Online March 2013 (http://www.scirp.org/journal/act)

Aberrations of the Cervical Carotid Artery Which May Be

Dangerous in Pharyngeal Surgery—A Computed

Tomographic Study

Johannes Gossner1,2, Ricarda Manka1,3, Joerg Larsen1,2

1Institute for Roentgendiagnostics, Braunschweig Teaching Hospitals, Braunschweig, Germany

2Department of Clinical Radiology, Weende Teaching Hospital, Göttingen, Germany

3Euradia, Private Radiology Practice, Braunschweig, Germany

Email: [email protected]

Received November 14, 2012; revised December 21, 2012; accepted January 4, 2013

ABSTRACT

Background: There are recognised variations in the anatomical course of the cervical portion of the internal carotid

artery. An aberrant vessel with direct contact to the pharyngeal wall could easily be injured during pharyngeal surgery

or may appear as a pharyngeal pseudo mass. Previous anatomical studies predominantly involved older patients. The

prevalence of such variations which are at risk of injury during pharyngeal surgery has thus not been established in a

general patient population. Material and Methods: The course of the internal carotid artery in relation to the oro and

hypopharyngeal walls was retrospectively evaluated bilaterally by simple visual inspection and measurement of the

smallest distance between the respective vessels and the adjacent mucosal surface of the pharyngeal wall in 138 con-

secutive contrast-enhanced computed tomography scans of the neck. Results: 11/138 (7.9%) of patients demonstrated

relevant cervical carotid artery aberrations, comprising medial kinking of a vessel with asymmetry of the adjacent pha-

ryngeal lumen and/or an intimate submucous course in the pharyngeal wall with no identifiable separating fat plane.

This prevalence increased with age. Simple visual inspection correlated well with the measurement of the smallest dis-

tance between an artery and the pharyngeal wall, which was statistically significant (p < 0.0001). Conclusions: The

prevalence of about 8% in a general patient population is higher than previously recorded in anatomical studies. Preva-

lence increases with age. Otorhinolaryngologists should be aware of such variation as a risk factor for haemorrhagic

complications during pharyngeal surgery and as a differential diagnosis of pharyngeal mass lesions, especially in older

patients. Modern contrast-enhanced CT allows identification and characterisation of any surgically relevant variant va-

scular anatomy in the pre-operative work-up.

Keywords: Computed Tomography; Internal Carotid Artery; Pharyngeal Surgery; Variant Anatomy

1. Introduction

Variations in the anatomical course of the cervical por-

tion of the internal carotid artery (ICA) are frequent and

reported to occur in about 6% - 30% of patients with

some authors even reporting a prevalence as high as 62%

(as reviewed by Ovchinnikov et al.) [1]. In most cases,

these are incidental findings lacking clinical relevance.

However, an aberrant ICA showing direct contact to the

pharyngeal wall could easily be injured during surgical

procedures, e.g., pharyngeal abscess drainage or tonsil-

lectomy [2]. Equally, it may appear as a mass lesion of

the pharynx, sometimes associated with clinical signs

such as dysphagia or globus syndrome [3-7]. For an ab-

errant cervical ICA which is at risk at surgery and/or

causing a pseudomass appearance, the term “dangerous

loop” has been proposed [8]. The previously performed

anatomical and angiographic studies mostly reported on

the anatomical variation per se, with some anatomical

studies recording the prevalence of the so called “dan-

gerous loop”. Anatomical studies on human cadavers

have the shortcoming of selection bias and naturally in-

volve older patients. The prevalence of clinically relevant

aberrations in a more general population is thus unclear.

Cross-sectional imaging offers an opportunity to study

human anatomy in vivo. With the use of intravenous con-

trast medium, the ICA can be easily identified and its

topographical relations studied. Such studies are part of

the routine investigations in almost any pre-surgical set-

ting. The present study has investigated the prevalence of

potentially dangerous variations of the cervical internal

carotid artery in a general patient population of a large

teaching hospital.

J. GOSSNER ET AL.

2. Material and Methods

Retrospective study of contrast-enhanced computed to-

mography (CT) scans of the neck performed between

October 2007 and February 2008 at the Institute of Ro-

entgendiagnostics at Braunschweig Teaching Hospitals.

According to the statute of the ethics of comittee of the

affiliated Hannover medical school (Medizinische Ho-

chschule) retrospective studies of available data are pos-

sible without dedicated statement. Patients were iden-

tified from the departmental RIS-data base and consid-

ered for inclusion into the study (n = 236). Patients with

mass lesions of the oro- or hypopharynx (such as ab-

scesses or malignancies) causing luminal asymmetry, any

history of cervical surgery (specifically neck dissection),

thrombosis of an ICA as well as intubated patients were

excluded from the analysis. Scans with excessive beam

hardening artefacts due to metallic dental implants were

also excluded. A total of 138 examinations were finally

included. The study population consisted of 91 men and

47 women (1.9:1) with an average age of 59.1 years (17 -

86 years). The 98 excluded patients had similar base-line

characteristics considering gender and mean age. Most

patients included in the study were being staged for va-

rious malignancies (lymphoma, breast cancer, melanoma,

head and neck tumours) or were examined to exclude a

clinical suspected parapharyngeal abscess.

A 16-slice CT scanner (Somatom®, Siemens Medical

Solutions, Germany) and an 8-slice CT scanner (Light-

Speed®, GE Healthcare, USA) were used. Scanning was

performed from the orbital floor to the upper thoracic

aperture at a slice thickness of 2 mm with the Siemens

and 1.25 mm with the GE-Scanner. 120 mL of non-ionic

iodinated contrast media (Ultravist®, Bayer-Schering,

Germany) was administered to each patient at a flow-rate

of 2 - 3 mL/s. For better arterial enhancement, a two-

phased acquisition was performed in most patients ac-

cording to standard departmental protocol: the contrast

medium volume was split into two portions (2 × 60 mL),

the second portion being administered 40 seconds fol-

lowing the first portion with scanning being started 60

seconds after the first injection of contrast medium. In

the remainder, a fixed delay of 60 seconds following in-

jection of contrast medium was used.

All scans were reviewed on transverse-axial recon-

structions in soft tissue window settings (WL 40 - 50,

WW 350) at a standard medical post-processing work-

station. CT studies were initially evaluated by simple vi-

sual inspection by a single observer who routinely re-

ports independently on cervical CT scans (JG). Any va-

riation in the course of an internal carotid artery was ju-

dged as potentially dangerous if it caused any asymme-

try of the oro or hypopharyngeal lumen and/or if the ICA

showed a direct sub-mucous course with no identifiable

separating fat plane to the pharyngeal wall. In patients

with a relevant anatomic variation, thin section multi-

planar reformations were performed for better depiction

of the topographic anatomy. To test the reliability of the

simple visual inspection assessment, the smallest dis-

tance between the internal carotids and the pharyngeal

lumen was finally measured in all patients by a second

examiner (RS). A cut-off value of ≤5 mm was chosen.

The accordance between patient with visually judged

“dangerous loop” and patients with a measured smallest

distance between the pharyngeal wall and the internal

carotids ≤5 mm was verified. The measured distances

between the grop with and without visually rated “dan-

gerous loop” were also compared using the t-test. For a

signifiant difference a p-value < 0.05 was defined. For

the calculation Statistica® was used (Version 5.5, ’99

Edition, StatSoft, USA).

3. Results

11 of 138 patients (7.9%) showed potentially dangerous

variations in the course of the cervical ICA, i.e. an asy-

mmetry of the lumen of the hypo- or oro-pharyngeal lu-

men and/or a direct sub-mucous course of the vessel with

no identifiable separating fat plane to the adjacent pha-

ryngeal wall (Figure 1). Their average age was 73.6

years (range 54 - 86 years) of whom 7 were men and 4

were women. One patient showed a sub-mucous course

of the carotid artery in isolation, while the luminal asy-

mmetry was only slight in two others. Prevalence in-

creased from 2% (2/99) in patients younger than 70 years

to 23.6% (9/38) in patients aged 70 or older.

All measurements in patients showing a potentially

dangerous variant were ≤5 mm (100%). Of the patients

Figure 1. Axial CT image of a 75-year-old man undergoing

staging of suspected cancer of the hard palate. There is me-

dial elongation of the right internal carotid artery associ-

ated with luminal asymmetry, the so called “dangerous

loop”.

J. GOSSNER ET AL. 31

with no obvious dangerous arterial variation on visual in-

spection, only 0.4% of all distance measurements were

≤5 mm. The mean distances between the two groups

were statistically significant (p < 0.0001).

4. Discussion

This study has investigated the occurrence of potentially

dangerous variations in the course of the cervical internal

carotid artery in a general patient population using con-

trast-enhanced cervical CT scans. Because surgical pro-

cedures are routinely performed in this area, such ana-

tomical variations are an obvious concern: A close con-

tact between an artery and the oro- or hypopharyngeal

wall may become a critical haemorrhagic risk at the time

of surgical interventions. For example, injury to an ICA

during tonsillectomy may result in life threatening blee-

ding [2]. On the other hand, these aberrations are an im-

portant differential diagnosis in the evaluation of pha-

ryngeal masses such as tumorous entities or abscesses

and any recognised variant anatomy may clearly alter pa-

tient management [2-8]. The differentiation of clinical

relevant and irrelevant variations is therefore of consid-

erable value, especially as relevant variations are de-

scribed in as much as 62% of patients [1]. It appears that

some elongation or kinking of the cranial portions of the

cervical segments of the carotid arteries is a normal com-

pensatory mechanism to prevent overstretching and nar-

rowing during movement of this important blood sup-

ply to the brain [1]. Prevalences of anatomic variants re-

corded in the literature are wide ranging from 5.3% to

62.4% (with n = 1123 [9], and n = 590 [10], respectively).

This may be explained by the use of different methods of

assessment, namely cadaveric, angiographic or ultrasono-

graphic studies in addition to different definitions of

what may constitute a clinically relevant variation. No

study has reported on findings from cross sectional im-

aging data. Finally, it is noteworthy that anatomical va-

riants as considered here may also be critically impor-

tant during neuroendovascular interventions such as stent-

protected carotid angioplasty or the coilembolisation of

intracranial aneurysms [11], however, these aspects are

beyond the scope of this study, which has focused so-

lely on potentially dangerous variants in the context of

pharyngeal surgery.

Few studies have considered surgically relevant varia-

tions of ICA anatomy, specifically a small distance be-

tween the ICA and the adjacent pharyngeal wall. Till-

mann and Christofides were first to report a prevalence

of 2.2% (2/89) in their anatomic study and proposed the

term “dangerous loop” [8]. Paulsen et al. studied the

course of the ICA in human cadavers. Kinking or coiling

with direct relation to the pharyngeal wall was noted in

2.8% (8/282) [12]. In another anatomical study by Ozgur

et al., 4% (2/50) of cases showed a direct relation be-

tween artery and the pharyngeal wall [13]. In our study,

we found a higher prevalence of 7.9%. This may in part

be explained by the different methodology: When using

fixation with formalin on human cadavers, some shrink-

ing of the tissue occurs which may alter parapharyngeal

topographic anatomy [14]. In contrast, cross-sectional

imaging allows the examination of human anatomy in

vivo. In a very recent study Jun et al. found a distance of

less than 5 mm between the internal carotid artery and

the hypopharyngeal wall in around 10% patients, which

is in accordance to our data. But they did not record mor-

phologic features of the “dangerous loop” like luminal

assymmetry or direct submucous course of the artery,

which is in our opinion a clinical relevant aspect [15]. In

addition, we have also excluded scans of patients in whom

pharyngeal anatomy was disturbed due to malignant or

inflammatory masses, intubation or postoperative changes

in order for observed pharyngeal asymmetry being solely

attributable to an aberrant course of an ICA. Some over-

diagnosis of patients showing luminal asymmetry could

have occurred because asymmetry may also be observed

during deglutition. However, the verification of a direct

submucous and thereby potentially dangerous course of

an ICA is independent of swallowing.

Where an ICA had an intimate relation to the adjacent

pharyngeal wall, the vessel was elongated and kinked

medially in all cases. The aetiology of this elongation

and kinking is not clear. Generally it is believed that

looping or coiling is due to congenital changes, whereas

elongation with kinking is acquired and ascribed to

atherosclerosis: a recent histological study of such a co-

hort described metaplastic changes of the ICA with a

reduction in elastic fibres and muscular cells, making the

vessel susceptible to haemodynamic forces such as in

arterial hypertension [16]. Elongation and unfolding of

the thoracic aorta have of course long been believed to be

due to long-standing hypertension [17]. More recently,

this observation has also been made for the carotid arter-

ies [10]. In addition, recently, Lam et al. reported an in-

creased prevalence of tortuosity of the common and in-

ternal carotid arteries with increasing age in their an-

giographic study of the vascular anatomy in patients un-

dergoing carotid angioplasty and stenting [11]. Progres-

sive kinking in relation to ageing has also been demon-

strated for the femoral artery [18]. In our sample, no case

of potentially dangerous elongation and kinking was

found in patients younger than 50 years and rarely oc-

curred in patients between 50 and 70 years of age, as

would be expected with an acquired condition.

The mean age of our patients was 59.1 years, with the

youngest being 17 years old. Our data can thus not be

easily applied to children, who commonly undergo pha-

ryngeal surgery, especially tonsillectomy. It is notewor-

J. GOSSNER ET AL.

thy therefore that Galetti et al. reported on an 8-year-old

child who complained of dysphagia and pharyngodynia

and was found to have kinking of the right ICA, giving

rise to an impression on the adjacent pharyngeal wall [2].

A possible explanation arises from the embryologic de-

velopment of the ICA from brachial arch arteries: a per-

sisting loop of the ICA could therefore be interpreted as a

rudimentary stage of development [11,12]. There are also

rare congenital syndromes with tortuosity of the great

vessels. However, these are usually accompanied by

other clinical stigmata such as skin and joint laxity in

Marfan’s syndrome [19], which should prompt further

consideration of vascular anomalies. As indicated above,

the published anatomical studies involved predominantly

older patients, so that no conclusions could be drawn for

younger patients. Nonetheless, the fact that no clinically

relevant anatomic variant of the ICA could be observed

in patients under the age of 50 years in our example as

well as the evidence for an acquired aetiology as cited

above makes a high prevalence of potentially dangerous

variations in children unlikely.

In our cohort, cervical CT scans with contrast en-

hancement demonstrated adequate depiction of carotid

anatomy in relation to the pharyngeal wall, similar to

previous reports [4-7]. CT imaging is a widely available,

robust, fast and accurate method of imaging carotid ves-

sel anatomy. The possibility of acquiring thin slices of-

fers the additional opportunity of high quality multi-

planar reformations. There are no contraindications like

pacemakers and even patients with claustrophobia are

usually examinable with CT. CT scans obtained for di-

agnostic purposes and pre-surgical planning can readily

be used for the study of the vascular anatomy. For better

depiction of the vascular anatomy and to obtain sufficient

parenchymal contrast, a split-bolus technique was used in

most patients in our study, a technique first described by

Platt and Gazer for abdominal imaging [20]. However, in

our experience, even a delayed enhancement provides

sufficient contrast to depict gross vascular pathology.

Nonetheless, there are several other imaging approaches

to demonstrate cervical vascular anatomy. MRI has the

advantage of lacking the use of ionising radiation, which

is particularly important when imaging children. Besides

from being generally less available, MRI has the short-

coming of longer scan times with more artefacts occur-

ring because of movement, specifically from respiration

and swallowing. MRI also commonly uses slice thick-

nesses in the 3 - 5 mm range, making the study of de-

tailed parapharyngeal anatomy problematic, and addi-

tional sequences such as MR-angiography may often be

required for full assessment. Especially older patient

frequently have contraindications like pacemakers. An

ultrasonographic examination has the advantage of being

an easy to use bed-side technique which allows the study

of the course of the ICA and possible variations thereof

[21]. In our opinion, ultrasound could easily be used as a

screening test, while cross-sectional imaging offers supe-

rior demonstration of the detailed topographical anatomy

which is needed for surgical planning. In contrast, con-

ventional angiography, apart from being an invasive

technique which carries the risk of occasionally deleteri-

ous consequences such as peri-procedural stroke, is not a

good choice for evaluating anomalies of the carotid ar-

teries since it neither shows the surrounding soft tissues

nor the relation of a vessel to the pharyngeal wall.

The simple visual judgement of ICA anatomy initially

applied in this study showed a good correlation with the

more objective measurement of the minimal distance

between the ICA and the pharyngeal lumen. All meas-

urements in patients showing a potentially dangerous

variation were ≤5 mm, in patients with no obvious clini-

cal variation no more than 0.4% had such a narrow rela-

tion. The measurements in the two groups were statisti-

cally significant (p < 0.0001). One might argue that only

the measured proximity between artery and mucosa is a

sufficient indicator for a dangerous aberration, however,

in everyday practice, any measurements are time con-

suming and checking for an asymmetry appears to us to

be a fair compromise when aiming to detect clinically

relevant carotid aberrations. In fact, all of the anatomical

studies cited above have solely used simple visual in-

spection and description of ICA anatomy following dis-

section since this is the standard method in macroscopic

anatomy [8-12]. Nonetheless, the judgement of topog-

raphical relations depends on the view point of the

anatomist and exact measurements of any alteration in

anatomy are clearly not easy to perform. These limita-

tions are overcome by the use of cross-sectional imaging

where multi-planar assessment of volume data sets as

routinely acquired in CT scanning is compulsory [22].

The patient sample was selected for the study of the

prevalence of potential dangerous variant anatomy of the

internal carotid artery. Patients with pathology disturbing

normal anatomy where excluded. So, in this sample there

was no direct impact on patient management. But, as a

consequence of this study the radiologists of the authors

department were sensitized of such dangerous variant

anatomy and we started to routinely comment on possi-

ble dangerous arterial variant anatomy in cervical CT-

scans.

In conclusion, potentially dangerous variant anatomy

of an internal carotid artery is seen in about 8% of cases

in a general patient population undergoing cervical CT

scanning. This prevalence is higher than that which has

been reported in anatomical studies previously. Preva-

lence increases with age in accordance with the proposed

degenerative aetiology. Otorhinolaryngologists and head

and neck surgeons should be aware of these variations as

J. GOSSNER ET AL.

a risk factor for major haemorrhage during pharyngeal

surgery and as a differential diagnosis in the considera-

tion of pharyngeal masses, specifically in the elderly.

Modern contrast-enhanced CT allows the identification

and characterisation of any surgically relevant variant

vascular anatomy in the pre-operative work-up, even if

delayed enhancement protocols are being used. Equally,

radiological reports on cervical CT scans should rou-

tinely comment on any such variant arterial anatomy.

5. Acknowledgements

An abstract of this study will presented as a poster at the

European Congress of Radiology in March 2013 at Vi-

enna.

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