From the Cerebrovascular Division, Department of Medicine, National
Cardiovascular Center, Osaka, Japan.
Correspondence to Masahiro Yasaka, MD, Cerebrovascular Division, Department of Medicine, National Cardiovascular Center, 5–7-1 Fujishirodai, Suita, Osaka 565-8565, Japan. E-mail yasakam{at}hsp.ncvc.go.jp
Methods—The subjects consisted of five healthy volunteers and
seven stroke patients. Examinations were performed with a color
Doppler flow imaging system equipped with convex array transducers
(7 or 9.5 MHz), originally designed for transrectal use. After local
anesthesia of the pharynx, we inserted a probe covered with
thin gum transorally, touching the tip to the pharyngeal posterolateral
wall. We then attempted to detect the ICA and measure flow velocity of
the distal extracranial ICA using principal images obtained by
TOCU.
Results—TOCU was successfully performed in all subjects without
any difficulty. In the healthy volunteers, the ICA was identified at a
depth of 2.2±0.6 cm and visualized as a vertical linear vessel
2.9±0.3 cm in length and bent slightly backward. The diameter and mean
flow velocity of the distal extracranial ICA were 4.7±0.2 mm and
50±7 cm/s, respectively. In the stroke patients, some remarkable
findings were obtained, including a narrow ICA with low flow velocity
in a patient with possible ICA dissection, a lucent echo without flow
signal in a patient with acute cardioembolic ICA occlusion, and
decreased ICA flow velocity in a patient with ipsilateral MCA
stenosis.
Conclusions—These preliminary data demonstrate the potential
applicability of TOCU to the evaluation of flow in the far distal
extracranial ICA. TOCU definitely warrants further investigation in
patients with carotid artery disease.
However, in patients with higher bifurcation of the
CCA,7 the mandibular bone prevents visualization
of the origin of the ICA.8 The course of the ICA
from the bifurcation to the skull base is not always straight but
occasionally curves strongly at its origin and on rare occasions is
coiled or kinked. The origin of the ICA is usually somewhat dilated,
and this widening extends up to 2 cm from the origin before the ICA
assumes a uniform diameter.8 Furthermore, reverse
flow at the ICA origin has been observed.1
Consequently, obtaining an appropriate size and location of sample
volume at the ICA origin can be difficult. In addition, measuring the
incident angle between blood flow and pulsed Doppler beam, allowing
determination of correct blood flow velocity, is occasionally
troublesome.
Conventional carotid ultrasonographic assessment of the distal
extracranial ICA is limited by the mandibular bone, even in patients
with a lower bifurcation, while far distal segments before the petrous
portion are often affected by pathological processes, such as
dissection, fibromuscular dysplasia, stationary arterial
waves, and hypoplasia of the ICA.8 9
In contrast, the ICA ascends vertically under the pharyngeal
posterolateral wall after branching from the CCA, and its pulse can be
easily felt by placing a finger on this wall. We used transoral carotid
ultrasonography (TOCU) to place a special probe on the pharyngeal
posterolateral wall and attempted to identify the distal extracranial
ICA and measure ICA flow velocity. We then assessed whether TOCU is
useful for evaluation of the distal extracranial ICA.
Examinations were performed with the use of a Toshiba SSA 260 A CDFI
system (Toshiba Inc) equipped with a 7-MHz convex array transducer
(PVL-625RT) and an ATL Ultramark 9 CDFI system (ATL Inc) equipped with
a 9- to 5-MHz convex array transducer (C9-5 ICT) (Figure 1
Informed consent was obtained from all subjects. After local
anesthesia of the pharynx was induced with the use of
lidocaine, the probe was inserted transorally, and the tip was touched
to the pharyngeal posterolateral wall (Figures 1
Using the CDFI system, we attempted to distinguish the ICA from
other vessels, such as the external carotid artery and its branches and
the jugular vein (Figure 3
Conventional Duplex carotid ultrasonography with linear array
probes (7.5 or 10 to 5 MHz) was also performed in all subjects on the
same day of TOCU examination. The flow velocities of the CCA and
proximal ICA were measured by an external approach and compared with
those of the distal extracranial ICA, which were obtained by a
transoral approach.
The correlation between the mean flow velocity of the CCA measured with
the use of both linear (10 to 5 MHz) and convex array (9 to 5 MHz)
transducers was examined in the 10 CCAs of five separate healthy
volunteers (men aged 32±4 years) with the use of the ATL Ultramark 9
CDFI system (ATL Inc) to elucidate whether differences in the frequency
and geometry of the ultrasound beams cause discrepancies in the
measured values of flow velocity.
Continuous data are expressed as mean±SD, and continuous variables
were analyzed with the use of the paired t test.
Statistical significance was established at the P<0.05
level.
In the healthy volunteers, the distal extracranial ICA was identified
at a depth of 2.2±0.6 cm and was visualized as a 2.9±0.3-cm-long
vertical linear vessel bent slightly backward (Table 2
In a stroke patient (patient 7), we compared enhanced CT findings with
those of TOCU (Figure 2
Although the results of the stroke patients were almost identical to
those of the healthy volunteers (Tables 2
Among all subjects, correlation between the mean flow velocities of the
CCA and ICA, when the ICA was determined by the transoral approach, was
high (r=0.82), whereas correlation was not high
(r=0.68) (Figure 6
No significant difference in the mean flow velocities of the CCA
measured with the linear and convex array transducers was observed
(49.1±8.6 cm/s and 48.6±9.1 cm/s, respectively;
P=0.62).
TOCU enables assessment of the arterial diameter and flow
velocity of the distal extracranial ICA, the site used for angiographic
measurement of diameter reduction in the North American
Symptomatic Carotid Endarterectomy
Trial and the Asymptomatic Carotid
Atherosclerosis Study.10 11 The
present findings suggest that TOCU may be useful in obtaining
accurate measurements of the diameter of the distal extracranial ICA,
particularly in patients with a high carotid bifurcation or kinking of
the proximal extracranial ICA.
In the present study, mean flow velocity measured by conventional
carotid ultrasonography with the use of the linear array transducer in
the proximal ICA was significantly lower than that measured by TOCU
with the use of the convex array transducer in the distal ICA, while no
difference in the mean flow velocities of the CCA measured by the
linear and convex array transducers was observed. Therefore, the
difference in the mean flow velocity at the proximal and distal ICA is
not due to difference in the frequency and geometry of the ultrasound
beams but is probably due to the diameter of the proximal ICA being
larger than that of the distal ICA8 while blood
flow volume is the same. When measuring flow velocity with high
reproducibility at the proximal ICA using conventional carotid
ultrasonography, we should put a sample volume at the point distal to
the CCA bifurcation at which the arterial walls become
parallel. However, in practice this is difficult because of
limited visualization of the proximal ICA by the mandibular bone, and
thus in the present study we were obliged to take measurements at
the somewhat dilated part of the proximal ICA.
The ICA origin is prone to atherosclerotic lesions, and carotid
ultrasonography with the use of the external approach is useful to
evaluate the quality and distribution of the
lesion.1 However, the distal end of the lesion is
sometimes difficult to confirm when an external approach is used, which
may make it difficult to determine indication of carotid
endarterectomy. At the very least, TOCU enables
easy evaluation of the distal extracranial ICA, although this procedure
cannot adequately demonstrate the carotid bifurcation.
We were able to identify the ICA in the patient with acute
occlusion of the right ICA but not in the patient with an old ICA
occlusion. The echogenicity of the thrombus may become as high as that
of the tissue surrounding the occluded artery, and thus the age of the
thrombus may be determined by the echogenicity of the ICA as
demonstrated by TOCU. In that case, identification of the ICA without
flow signal may indicate a recent occlusion, and failure to make such
an identification because of increased echogenicity may indicate an old
occlusion.
Recently, Kimura et al4 reported mobile echogenic
intravascular structures at the ICA origin in patients with acute
cardioembolic stroke, which were considered to be thrombi extended from
the distal end of the ICA, where emboli are prone to lodge. Although
such mobile echogenic intravascular structures were not detected by
TOCU in our patient with cardioembolic stroke (patient 2), in the
future, retrograde extension of the thrombi from the top of the ICA may
be demonstrated with the use of serial TOCU examinations in the acute
phase of cardioembolic ICA occlusion.
We examined two patients with suspected old ICA dissection. The
lesion in one patient was limited to the ICA origin, but that in the
other was located along the entire ICA. In the latter case, TOCU
demonstrated a narrow ICA at the cervical portion, which was
consistent with angiographic findings probably due to the
dissection. Carotid Doppler sonography has been able to provide
early recognition of ICA dissection and monitoring of
ICA.12 Therefore, TOCU may contribute to
evaluating the distribution of an ICA dissection in its acute
phase.
The transoral approach was introduced by Keller et
al13 in 1976. They used a bidirectional
continuous-wave Doppler ultrasound system to detect flow in the
vertebral arteries. However, to our knowledge, ours is the first report
to describe evaluation of the ICA by the transoral approach with
continuous-wave Doppler, B-mode, or CDFI.
In conclusion, these preliminary data illustrate the potential
applicability of TOCU to evaluate flow in the far distal extracranial
ICA. This method definitely warrants further examination in patients
with carotid artery disease.
Received December 10, 1997;
revision received April 7, 1998;
accepted April 7, 1998.
2.
Handa N, Matsumoto M, Maeda H, Hougaku H, Kamada T.
Ischemic stroke events and carotid
atherosclerosis: results of the Osaka follow-up
study for ultrasonographic assessment of carotid
atherosclerosis (the OSACA study). Stroke. 1995;26:1781–1786.
3.
Kagawa R, Moritake K, Shima T, Okada Y. Validity of
B-mode ultrasonographic findings in patients undergoing carotid
endarterectomy in comparison with angiographic and
clinicopathologic features. Stroke. 1996;27:700–705.
4.
Kimura K, Yonemura K, Terasaki T, Hashimoto Y, Uchino
M. Duplex carotid sonography in distinguishing acute unilateral
atherothrombotic from cardioembolic carotid artery occlusion.
AJNR Am J Neuroradiol. 1997;18:1447–1452.[Abstract]
5.
Yasaka M, Omae T, Tsuchiya T, Yamaguchi T. Ultrasonic
evaluation of the site of carotid axis occlusion in patients with acute
cardioembolic stroke. Stroke. 1992;23:420–422.
6.
Androulakis AE, Labropoulos N, Allan R, Tyllis TK,
Kutoubi AAI, Nicolaides AN. The role of common carotid artery
end-diastolic velocity in near total or total internal
carotid artery occlusion. Eur J Vasc Endovasc Surg. 1996;11:140–147.[Medline]
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7.
Huber P. Common carotid artery. In: Huber P, ed.
Krayenbühl/Yasargil Cerebral Angiography. Stuttgart,
Germany: Georg Thieme Verlag; 1982:36–37.
8.
Mohr JP, Gautier JC, Pessin MS. Internal carotid
artery disease. In: Barnett HJM, Mohr JP, Stein BM, Yatsu FM,
eds. Stroke: Pathophysiology, Diagnosis, and Management. New
York, NY: Churchill Livingstone; 1992:285–335.
9.
Huber P. Pathological changes of the internal carotid
artery. In: Huber P, ed. Krayenbühl/Yasargil Cerebral
Angiography. Stuttgart, Germany: Georg Thieme Verlag; 1982:55–61.
10.
North American Symptomatic Carotid
Endarterectomy Trial Collaborators. Beneficial
effect of carotid endarterectomy in
symptomatic patients with high-grade carotid
stenosis. N Engl J Med. 1991;325:445–453.[Abstract]
11.
Executive Committee for the Asymptomatic
Carotid Atherosclerosis Study:
Endarterectomy for asymptomatic carotid
artery stenosis. JAMA. 1995;273:1421–1428.
12.
Steinke W, Rautenberg W, Schwartz A, Hennerici M.
Noninvasive monitoring of internal carotid artery dissection.
Stroke. 1994;25:998–1005.[Abstract]
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Keller HM, Meier WE, Kumpe DA. Noninvasive angiography
for the diagnosis of vertebral artery disease using Doppler
ultrasound (vertebral artery Doppler). Stroke. 1976;7:364–369.
© 1998 American Heart Association, Inc.
Original Contributions
Transoral Carotid Ultrasonography
Abstract
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Background and Purpose—We attempted
ultrasonographic evaluation of the distal extracranial internal carotid
artery (ICA) using the transoral method (transoral carotid
ultrasonography [TOCU]).
Key Words: carotid artery diseases • cerebrovascular disorders • ultrasonography, Doppler
Introduction
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
Carotid
ultrasonography with CDFI has enabled the evaluation of plaques or
occlusive diseases at the extracranial carotid arteries by B-mode
imaging, color flow imaging, and measurement of flow
velocity.1 2 3 4 It has also contributed to the
assessment of occlusive diseases of distal arteries, such as occlusions
at the top of the ICA or the main trunk of the MCA, by comparing
bilateral flow velocities obtained from the
CCAs.5 6
Subjects and Methods
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
The subjects consisted of five healthy volunteers (aged 33±5
years) and seven stroke patients (aged 61±14 years). The demographic
profiles of the stroke patients are summarized in Table 1
.
View this table:
[in a new window]
Table 1. Demographics of Stroke
Patients ). These transducers were
originally designed for transrectal use. We covered the probes with
disposable sterile thin gum after covering the tip of the probe with
echo jelly.
View larger version (131K):
[in a new window]
Figure 1. Top, Side view of the probe (C9-5 ICT). Left
bottom, Tip of the probe. Right bottom, Tip of the probe was touched to
the left pharyngeal posterolateral wall transorally in a healthy
volunteer. 
and 2).
View larger version (96K):
[in a new window]
Figure 2. Left, Horizontal plane enhanced CT image at the
level of the pharynx in patient 7. Right, Short-axis view of the CDFI
obtained with TOCU in the same patient. TNG indicates tongue; TNS, left
tonsil; E, external carotid artery; I, internal carotid artery; and V,
jugular vein. The arrowhead indicates placement of the tip of the
probe. ). We
identified an ICA by delineation of a vessel running linearly from the
lower to the higher pharynx and by confirming that flow was proceeding
upward to the skull base, that the flow velocity pattern was identical
to that of the ICA, and that branching was absent. We determined the
characteristics of TOCU color flow images of the distal extracranial
ICA and measured the length, depth (from the surface of the posterior
wall to the anterior wall of the ICA), diameter, and flow velocity of
the distal extracranial ICA.
View larger version (122K):
[in a new window]
Figure 3. CDFI and Doppler waveforms of a healthy
volunteer. Left, Short-axis views obtained at the right pharyngeal
upper (top) and lower (bottom) posterior wall. Middle, Long-axis views
at the lines of a (top), b (middle), and c (bottom) indicated on the
short-axis views. Right, Doppler waveforms of the ICA (top),
jugular vein (middle), and external carotid artery (bottom). E
indicates external carotid artery; I, internal carotid artery; and V,
jugular vein.
Results
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
TOCU was performed in all subjects without difficulty. However,
most subjects needed to spit two or three times during and after the
examination. ). The diameter of the
distal extracranial ICA (4.7±0.2 mm) was significantly smaller
than that of the proximal ICA (5.6±0.9 mm; P<0.001).
The bifurcation of the CCA could not be visualized with the use of
TOCU. Correction of the incident angle between the ICA and Doppler
beam was easily performed because the incident angle was 60° or less
in all cases. The mean flow velocity (50±7 cm/s) of the distal
extracranial ICA obtained by the transoral approach was significantly
higher (P<0.01) than that of the proximal ICA (37±8 cm/s)
by the external approach and as high as that (54±8 cm/s) of the CCA.
The side-to-side ratio of the mean flow velocity of the distal
extracranial ICA was calculated by dividing the mean flow velocity of
the faster side by that of the slower side and was 1.17±0.03. The
pulsatility index (0.7±0.1) of the distal extracranial ICA
recorded by the transoral approach was lower than those of the CCA
(1.7±0.3) and proximal ICA (1.0±0.4) as determined by the external
approach (P<0.01 and P=0.051, respectively).
View this table:
[in a new window]
Table 2. Dimensions of ICAs as Determined by
TOCU ) and found that the locations of the ICA,
external carotid artery, and jugular vein corresponded well between the
two methods. and 3), there were some
remarkable findings associated with various pathologies. In one patient
(patient 1) who was suspected of having a right ICA dissection, the
right ICA was evident as a narrow signal with low flow velocity (Figure 4), which was consistent with cerebral
angiographic findings. In a patient (patient 2) with acute
cardioembolic ICA occlusion 3 days after stroke onset, confirmed by
right CCA angiography (Figure 5), the right ICA was
visible on a TOCU-obtained B-mode image but did not show any flow
signal, while the left ICA flow was normal. In contrast, we were unable
to demonstrate the occluded right ICA either on a B-mode image or on
CDFI in a patient (patient 5) with atherothrombotic right ICA occlusion
confirmed by angiography. In a patient with stenosis of the
right MCA (patient 3), the ICA flow velocity of the affected side (57
cm/s) was lower than that (82 cm/s) of the nonaffected side. The
side-to-side ratio (82/57=1.44) was higher than 1.23 (mean+2SD of the
side-to-side ratio in the control subjects).
View this table:
[in a new window]
Table 3. Mean Velocity and Pulsatility Index of the CCA
and
ICA
View larger version (106K):
[in a new window]
Figure 4. Angiographic images of early (A) and late (B)
arterial phases after the same right CCA injection in the
patient with a clinical diagnosis of right ICA dissection (patient 1),
and CDFI and Doppler waveforms of the right ICA (C and D) and the
left ICA (E and F). Arrow indicates the right ICA; arrowhead, the right
external carotid artery.
View larger version (105K):
[in a new window]
Figure 5. Left, Right CCA angiography of the patient with
cardioembolic right ICA occlusion (patient 2, arrow); middle, B-mode
image of the right ICA (*) of the same patient; right, CDFI of the left
ICA (arrow) of the same patient. ) when the
ICA was assessed by the external approach.
View larger version (14K):
[in a new window]
Figure 6. Relationship between CCA and ICA mean flow
velocity measured by the external approach (left) and the transoral
approach (right). Two values are plotted at the same point (42, 56) in
the graph on the right.
Discussion
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
The ICA runs so linearly and superficially under the pharyngeal
posterolateral wall that sufficient length of the distal extracranial
ICA can be evaluated to allow accurate flow velocity measurement. This
may explain the high correlation observed between the mean flow
velocities of the CCA and ICA determined by the transoral approach.
Selected Abbreviations and Acronyms
CCA
=
common carotid artery
CDFI
=
color Doppler flow imaging, color Doppler flow image
ICA
=
internal carotid artery
MCA
=
middle cerebral artery
TOCU
=
transoral carotid ultrasonography
Acknowledgments
This study was supported in part by research grants for
cardiovascular disease (8C-4, 9A-2, 9A-3, 9A-8) from
the Ministry of Health and Welfare of Japan and by the special
coordination funds for promoting science and technology (Strategic
Promotion System for Brain Science) from the Science and Technology
Agency of Japan.
References
Top
Abstract
Introduction
Subjects and Methods
Results
Discussion
References
1.
Hennerici M, Rautenberg W, Mohr JP, Steinke W.
Ultrasound imaging and Doppler sonography in the diagnosis of
cerebrovascular diseases. In: Barnett HJM, Mohr JP, Stein BM, Yatsu FM,
eds. Stroke: Pathophysiology, Diagnosis, and Management. New
York, NY: Churchill Livingstone; 1992:241–269.
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