| Revised: 10 February 2018 | Accepted: 4 April 2018

DOI: 10.1002/jcu.22599

CASE REPORT

Contrast-enhanced transoral carotid ultrasonography for the
evaluation of plaque protrusion after carotid artery stenting
Yuta Hagiwara MD1

|

Tomohide Yoshie MD2 | Takahiro Shimizu MD1 |

Takayuki Fukano MD2 | Tatsuro Takada MD2 | Toshihiro Ueda MD2 |
Yasuhiro Hasegawa MD1
1
Department of Internal Medicine, Division
of Neurology, St. Marianna University
School of Medicine, Kawasaki, Japan
2

Abstract
A 67 year-old man was admitted to our hospital because of mild left hemiparesis and was diag-

Department of Strokology, Stroke Center,
St. Marianna University Toyoko Hospital,
Kawasaki, Japan

nosed with cerebral infarction caused by right internal carotid artery stenosis. He was treated with

Correspondence
Yuta Hagiwara, Department of Neurology,
St. Marianna University School of Medicine,
2-16-1, Sugao, Miyamae-ku, Kawasaki
216-8511, Japan.
Email: [email-masked]

postoperative angiogram suggested protrusion in the stent, which could not be seen on conven-

dual antiplatelet therapy and scheduled for carotid artery stenting 14 days after onset. The preoperative right carotid angiogram showed 60% stenosis by the NASCET criteria, with an ulcer. The
tional carotid ultrasonography because of its high location. On transoral carotid ultrasonography,
clear delineation of the lesion was not possible due to color blurs. Contrast-enhanced transoral
carotid ultrasonography (CETOCU) clearly demonstrated the protrusion and delineated the lumen
within the stent.
KEYWORDS

contrast-enhanced ultrasonography, internal carotid artery, stenosis, stenting, transoral approach

1 | INTRODUCTION

therapy, and he was scheduled for CAS 14 days after onset. We chose
CAS rather than endarterectomy because the stenotic lesion was

Transoral carotid ultrasonography (TOCU) is a useful imaging modality

located very distally.

for diagnosis of extracranial internal carotid artery (ICA) lesions.1

Because of the length of the stenotic lesion, we planned to use

Contrast-enhanced transoral carotid ultrasonography (CETOCU) pro-

two stents. We placed the first stent (carotid Wall-stent 10 mm 3

vides a clear intraluminal image of the distal extracranial ICA that can-

31 mm; Boston Scientific, Natick, Massachusetts) after balloon predila-

not be reached from the neck.2–4 We report the case of a patient with

tion, then a second stent (Precise 7 mm 3 30 mm; Johnson & Johnson,

plaque protrusion after carotid artery stenting (CAS), in whom

Cordis, Miami, FL). We did not perform balloon post-dilation. The

CETOCU offered clear and detailed images of the protrusion.

carotid angiogram immediately after stenting suggested plaque protrusion within the stents (Figure 2). Since the protrusion was observed
immediately after the stent placement, a newly developed plaque or a

2 | CASE PRESENTATION

thrombus within the stent seemed unlikely. 3D-CT angiography (CTA)
A 67-year-old man with no remarkable previous personal or family

on the day after CAS showed two protrusions in the stents (Figure 3).

medical history was admitted to our hospital because of mild left hemi-

Conventional carotid ultrasonography failed to demonstrate the lesions

paresis. Magnetic resonance imaging (MRI) showed multiple cerebral

because of their distal location and poor rendering of color-Doppler

infarctions in the right watershed area. He was diagnosed with cerebral

imaging in the stent lumen. TOCU with color-Doppler was performed,

infarction caused by right ICA stenosis and treated with dual antiplate-

but did not clearly show the protrusions because the lesions were

let therapy. The preoperative carotid angiography confirmed the pres-

hypo-echoic (Figure 4). On the contrary, CETOCU clearly demonstrated

ence of an ulcerated atherosclerotic plaque producing 60% stenosis

plaque protrusions inside the stents (Figure 5 and video-clip). It enabled

according to the North American Symptomatic Carotid Endarterectomy

to evaluate in detail the size, morphology, and position of the protru-

Trials (NASCET) method (Figure 1). His symptoms recovered after

sions. Based on the CETOCU images, anticoagulation was started in

J Clin Ultrasound. 2018;1–4.

wileyonlinelibrary.com/journal/jcu

C 2018 Wiley Periodicals, Inc.
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HAGIWARA ET AL.

Right carotid angiogram before carotid artery stenting. A, Anteroposterior view. B, Lateral view. Right carotid angiogram shows
60% stenosis of the right internal carotid artery by NASCET criteria, with an ulcer

FIGURE 1

addition to the dual antiplatelet therapy to prevent secondary throm-

3 | DISCUSSION

bus formation and occlusion. The patient remained asymptomatic, and
the protrusions diminished. Thus, the patient was discharged 14 days

Contrast-enhanced carotid ultrasound (CEUS) with perfluorobutane

after CAS.

microbubbles as a contrast agent can be used to assess the stability of

Right carotid angiogram after carotid artery stenting. A, Anteroposterior view. B, Lateral view. Right carotid angiogram after
stenting suggesting plaque protrusion within the stent

FIGURE 2

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HAGIWARA ET AL.

3-D CT angiography (CTA) of the right carotid artery
after stenting, lateral view. CTA after stenting shows two plaque
protrusions in the stent. There is a small protrusion at the
bifurcation of the carotid artery, and the distal protrusion is larger
than the proximal one

FIGURE 3

carotid atherosclerotic plaques.5 While CEUS is used to evaluate plaque stability, CETOCU, like CT and carotid angiography, is used to
observe the vessels themselves. Moreover, it is capable of clearly visualizing hypoechoic lesions. Depending on the location of the lesion,
CETOCU may deliver a more useful image than carotid angiography
with the advantage of being less invasive.
Plaque protrusion in the stent is one of the serious complications
that can lead to cerebral infarction after CAS. Intravascular ultrasound
(IVUS) and CTA are currently the most used modalities for the evalua-

Contrast-enhanced transoral carotid ultrasonography
(CETOCU) of the right carotid artery after stenting, with schematic
images. Compared to the transoral carotid ultrasonography with
color Doppler imaging shown in Figure 5, CETOCU clearly
demonstrates the proximal and distal protrusions in the stent
(video clip)

FIGURE 5

tion of plaque protrusion in stents.6–8 Although these imaging modalities are minimally invasive, they cannot be repeated within a few days.

exposure to radiation in CETOCU. Moreover, CETOCU can be repeat-

The advantages of CETOCU over CTA are that it is less-invasive, and

edly performed with simple preparation at the bedside, even if the

the contrast agent is non-nephrotoxic and less allergenic than the CT

patient has renal impairment.

contrast agent. Unlike CTA and carotid angiography, there is no

Conventional TOCU is well suited to observing lesions located in
the upper extracranial ICA,1 from the carotid bifurcation to the second
cervical vertebra. It has the advantages of bedside availability, absence
of exposure to radiation, minimal invasiveness, lower cost, and absence
of significant contraindication. TOCU is particularly useful for patients
with high-located carotid bifurcation. However, conventional colorDoppler imaging remains poor within the stent, and hypoechoic lesion
can be missed or improperly delineated. On the contrary, contrastenhanced TOCU offers a clear delineation between the plaque protrusion and the vessel lumen.
CETOCU is a useful method to evaluate plaque protrusion in
stents, where it is preferable to repeated carotid angiograms and CTA.

Transoral carotid ultrasonography (TOCU) with color
Doppler imaging of the right carotid artery. TOCU of the right
carotid artery after stenting suggests plaque protrusion in the
middle of stent. However, the proximal protrusion detected by
CTA is not visible

FIGURE 4

E THIC AL AP PR OVAL
All procedures followed were approved by the St. Marianna University
Bioethics Committee and performed in accordance with the Helsinki
Declaration of 1964 and later versions.

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HAGIWARA ET AL.

IN FORME D CONS ENT
Informed consent was obtained from the patient for inclusion in this

extracranial internal carotid artery dissection: A case report. J Clin
Ultrasound. 2017;1–4.
[4] Hagiwara Y, Yoshie T, Shimizu T, et al. Contrast-enhanced transoral
carotid ultrasonography for the evaluation of a long stenotic lesion in
the internal carotid artery. Clin Case Rep. 2016;4(12):1215.

study.

C ONFLICT OF INT E RE ST
The all authors have no conflicts of interest to declare.
DI SCLOSU RE
Dr. Yuta Hagiwara reports no disclosures.
Dr. Tomohide Yoshie reports no disclosures.
Dr. Takahiro Shimizu reports no disclosures.
Dr. Takayuki Fukano reports no disclosures.
Dr. Tatsuro Takada reports no disclosures.
Dr. Toshihiro Ueda reports no disclosures.

[5] Saito K, Nagatsuka K, Ishibashi-Ueda H, et al. Contrast-enhanced
ultrasound for the evaluation of neovascularization in atherosclerotic
carotid artery plaques. Stroke. 2014;45(10):3073.
[6] Shinozaki N, Ogata N, Ikari Y. Plaque protrusion detected by intravascular ultrasound during carotid artery stenting. J Stroke Cerebrovasc Dis. 2014;23(10):2622.
[7] Hashimura N, Mutoh T, Matsuda K, et al. Evaluation and management of plaque protrusion or thrombus following carotid artery
stenting. Neurol Med Chir. 2015;55(2):149.
[8] Misaki K, Uchiyama N, Mohri M, et al. Prediction of carotid artery instent restenosis by quantitative assessment of vulnerable plaque
using computed tomography. J Neuroradiol. 2016;43(1):18.

Dr. Yasuhiro Hasegawa reports no disclosures.
SUP POR TI NG INFOR MATION

OR CID
Yuta Hagiwara MD

http://orcid.org/0000-0002-3420-4218

Additional Supporting Information may be found online in the supporting information tab for this article.

R E FER E NCE S
[1] Yasaka M, Kimura K, Otsubo R, et al. Transoral carotid ultrasonography. Stroke. 1998;29:1383.
[2] Hagiwara Y, Yoshie T, Shimizu T, et al. A case in which contrast-enhanced
transoral carotid ultrasonography was useful for pre- and post-procedural
evaluation in carotid artery stenting. J Med Ultrason. 2017;44(2):207.
[3] Hagiwara Y, Shimizu T, Hasegawa Y. Contrast-enhanced transoral
carotid ultrasonography for the diagnosis and follow-up of

How to cite this article: Hagiwara Y, Yoshie T, Shimizu T, et al.
Contrast-enhanced transoral carotid ultrasonography for the
evaluation of plaque protrusion after carotid artery stenting.
J Clin Ultrasound. 2018;00:1–4. https://doi.org/10.1002/jcu.
22599