Diagnostic vascular ultrasonography with

the help of color Doppler and

contrast-enhanced ultrasonography

Johannes Rübenthaler, Maximilian Reiser, Dirk-André Clevert

REVIEW ARTICLE
Department of Clinical Radiology, Ludwig-Maximilians-University of Munich-Grosshadern
[Link]
Campus, Munich, Germany pISSN: 2288-5919 • eISSN: 2288-5943
Ultrasonography 2016;35:289-301

The use of ultrasonography and especially of contrast-enhanced ultrasonography (CEUS) in

the diagnosis of vascular pathologies before and after interventions has significantly increased
over the past years due to the broader availability of modern ultrasound systems with CEUS Received: May 26, 2016
capabilities and more trained user experience in this imaging modality. For the preinterventional Revised: August 12, 2016
Accepted: August 12, 2016
and postinterventional work-up of carotid diseases, duplex ultrasound as well as CEUS have
Correspondence to:
been established as the standard-of-care examination procedures for diagnosis, evaluation, and Dirk-André Clevert, MD, Department of
follow-up. In addition to its use for carotid arterial diseases, ultrasonography has also become Clinical Radiology, Munich University
Hospital, Marchioninistr. 15, 81377
the primary modality for the screening of vascular pathologies. This review describes the most Munich, Germany
common pathologies found in ultrasonography of the carotid arteries, the abdominal aorta, and Tel. +49-89-44007-3620
the femoral arteries. Fax. +49-89-44007-8832
E-mail: [Link]@[Link]-
[Link]
Keywords: Contrast media; Ultrasonography, contrast-enhanced; Carotid stenosis; Arteriovenous
fistula; Dissection; Plaque, atherosclerotic

This is an Open Access article distributed under the

terms of the Creative Commons Attribution Non-
Introduction Commercial License ([Link]
licenses/by-nc/3.0/) which permits unrestricted non-
commercial use, distribution, and reproduction in
any medium, provided the original work is properly
The initial diagnostic workup of patients suspected of suffering from carotid artery disease is duplex cited.
ultrasonography of the carotid vessels (Fig. 1) [1-7]. Duplex ultrasonography is also the preferred
imaging modality for the follow-up of patients after stent implantation or endarterectomy [8,9]. Copyright © 2016 Korean Society of
Ultrasound in Medicine (KSUM)
Among patients showing amaurosis fugax or hemispheric transient ischemic attacks, 88% reveal
atherosclerotic plaques at the carotid bifurcation [10] and about 25%-50% of all strokes are a result
of ruptured atherosclerotic plaques; in addition, about 80% of all strokes are of ischemic origin [11-
13]. Internal carotid artery (ICA) stenosis quantification is essential for the clinical management of
patients, since several trials have concluded that symptomatic patients with high-grade stenosis
(70%-90%) of the ICA, as well as asymptomatic patients with high-grade stenosis, benefit from
carotid endarterectomy (CEA) [14-18].
In abdominal ultrasonography, abdominal aortic aneurysms (AAAs) are found in 2% to 8% of How to cite this article:
Rübenthaler J, Reiser M, Clevert DA.
men over the age of 65 years, with incidence in women that is lower by a factor of 4 [19]. All AAAs Diagnostic vascular ultrasonography with the
are defined as an enlargement of the abdominal aorta greater than 3.0 cm or greater than 50% of help of color Doppler and contrast-enhanced
ultrasonography. Ultrasonography. 2016
normal size [19]. About 85% of all AAAs are detected below the origin of the kidney vessels [19]. Oct;35(4):289-301.

[Link] Ultrasonography 35(4), October 2016 289

 Johannes Rübenthaler, et al.

A B C
Fig. 1. Ultrasonography of a carotid bulb.
A, B. B-Scan (A) and color Doppler (B) sonograms of the carotid bulb demonstrate the distal common carotid artery (asterisk), the proximal
internal carotid artery (ICA) (arrow) and external carotid artery (ECA) (arrowhead). C. Contrast-enhanced ultrasonography of the carotid bulb
demonstrates the perfused lumen of distal common carotid artery, the proximal ICA and ECA.

Surgical intervention is recommended at any diameter greater reflect an echo with an amplified echo intensity of up to 30 dB
than 5.5 cm in men or 5.0 cm in women [19]. The main risk is a [35,37]. Major side effects must be taken into consideration, which
rupture, with a risk of less than 1% for aneurysms with a size of are comparable to those of contrast agents used for other imaging
less than 5.5 cm, 10% for aneurysms with a diameter between 5.5 modalities. The most important possible side effect of an ultrasound
cm and 7.0 cm, and 33% for aneurysms larger than 7.0 cm [19]. A contrast agent is an anaphylactic reaction, which is described to
ruptured AAA shows a mortality rate of 85% to 90% [19]. Clinical occur in one out of 10,000 cases [38,39].
management includes conservative treatment with follow-up SonoVue (Bracco, Milan, Italy), most commonly used among
ultrasonography for asymptomatic AAAs with a diameter less than modern ultrasonography contrast agents, consists of phospholipid
5.5 cm, as there is a higher risk of peri-interventional complications shells, which stabilize microbubbles, and their core, containing
than of rupture and surgical repair for AAAs above that size, with sulphur hexafluoride (SF6) gas. Once administered, the ultrasound
contrast-enhanced ultrasonography (CEUS) follow-up examinations contrast agent is quickly eliminated. The phospholipids are
after endovascular aneurysm repair (EVAR) [20-28]. metabolized endogenously and the SF6 gas is exhaled via the
Duplex ultrasonography is also the imaging modality of choice lungs within a time period of up to 8 minutes. At 2-10 µm, a
for the detection of complications after puncture of the femoral single microbubble is about the size of an average erythrocyte. For
artery, as they occur in 0.1%-9% of cases with aneurysms, with diagnostic views of the vessels, 1.6 to 2.4 mL of contrast agent
arteriovenous fistulas, dissections, and hematomas being the most should be intravenously administered as a bolus injection, followed
common complications [29-34]. by a flush of 5-10 mL of saline solution (0.9% NaCl) in order to
achieve good contrast [40].
Contrast-Enhanced Ultrasonography Technique
Carotid Arterial Diseases
With the implementation of specific contrast modes in modern
ultrasound systems and the broader availability of these systems in Stenosis
the clinical routine, CEUS can be used for the assessment of vascular About 10%-15% of all strokes and transitory attacks of ischemic
complications. Modern contrast modes use a low mechanical origin are the consequence of an atherosclerotic stenosis of the
index mode that processes the non-linear signals emitted by the ICA, especially of the proximal part [41]. Most important in the
microbubbles of the contrast agent and separates out the signals initial workup of ICA stenosis is the differentiation between
of the tissue and the contrast agent [35,36]. The contrast agent is a total occlusion of the ICA or a preocclusive stenosis that is
intravenously administered through a needle of at least 18G. The characterized as a stenosis of at least 90% [42-47]. Preocclusive
microbubbles oscillate in response to the emitted ultrasound and symptomatic stenosis can be treated with surgical intervention or

290 Ultrasonography 35(4), October 2016 [Link]

CEUS in vascular diseases

with other interventional measures in order to prevent a threatening Carotid artery stenting (CAS) is an alternative to the traditional
hemiparesis [3,6]. With sensitivities between 86% and 98% and CEA, especially in patients with a high risk of complications
specificities between 87% and 100%, vascular ultrasonography of from undergoing surgery, for example, patients with significant
the ICA has a high diagnostic accuracy in the characterization of cardiopulmonary disease [57-59]. The use of CEA carries a risk of
ICA stenosis and in the differentiation of ICA occlusions, dependent restenosis of about 25%, whereas the risk of restenosis after CAS is
on examiner experience and parameter settings [48-50]. With below 5% in most cases in the initial 5 years after stenting [9,60-
CEUS, it is even possible to advance the visualization of carotid 63]. Duplex ultrasonography and CEUS are the imaging modalities
artery diseases by detecting the blood flow through the stenosis of choice for postinterventional surveillance for restenosis after CAS
even in elongated vessels, without the disadvantage of an angle and for the characterization of in-stent restenosis after stenting,
dependency or aliasing or blooming flow artifacts (Fig. 2) [51-55]. with CEUS providing a reduction of flow artifacts and a better
visualization of the morphology of the restenosis compared to color
Postinterventional Follow-up and power Doppler (Fig. 3) [64-66].
The traditional method of choice for the treatment of symptomatic
and asymptomatic patients with ICA stenosis is the CEA [47,56].

A B

C D
Fig. 2. Ultrasonography of a 67-year-old woman with recent ischemic neurological symptoms.
A. B-Scan shows a high-degree internal carotid artery (ICA) stenosis with soft plaques (arrow). B, C. Duplex ultrasonography shows a high-
degree stenosis of the ICA (arrowhead) with a maximal systolic flow velocity of about 500 cm/sec. D. Contrast-enhanced ultrasonography
(CEUS) detects the intrastenotic flow (arrowhead) without overwriting the wall of the vessel and reveals the complete residual lumen and
the length of the stenosis. Additionally, CEUS confirms the absence of intraplaque neovascularization (arrow).

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 Johannes Rübenthaler, et al.

Dissection Complications after Intervention

Cervical dissections are rather uncommon and can be divided into With an incidence of about 2%-10%, the puncture of the carotid
spontaneous or traumatic dissections. The annual incidence of artery is the most common complication after central venous
dissections is about 1-3 out of 100,000 cases, and they account for catheterization of the internal jugular vein [74,75]. This intervention
15%-20% of all cerebral infarctions in adolescents [67]. Clinical is mostly performed at the intensive care unit or for interventional
symptoms of dissections vary acutely from individual to individual radiological procedures. The most important complication is
[68]. Vascular ultrasonography is the imaging modality of choice for an arteriovenous fistula that can occasionally be seen clinically
the detection and characterization of acute dissection by imaging as a swelling of the neck, sometimes pulsatile [76]. Duplex
the mural hematoma as well as the false and true lumen, along ultrasonography and CEUS are the imaging modalities of choice for
with the normal visualization of a decreased blood volume flow the detection of arteriovenous fistulae, with CEUS being the superior
in the false lumen that results in an increased risk for thrombosis, imaging technique because of its independence from aliasing or
embolization, or even partial or total occlusion of the artery [69-71]. overwriting artifacts (Fig. 4) [5,77,78].
Modern ultrasound probes can even identify a small dissection with
very thin membranes of less than 1 mm [4,72,73]. The use of CEUS Plaque Characterization
can aid diagnosis and improve diagnostic accuracy in difficult cases Ulcerating plaques are thought to be a factor in the aetiology of
[51,53]. strokes from carotid arterial diseases [79,80]. The use of CEUS is an
imaging modality option for detecting plaque ulceration that might

A B

C D
Fig. 3. Longitudinal ultrasonography after internal carotid artery (ICA) stent insertion.
A. B-Scan shows an ICA stent (arrowheads). B. Power Doppler ultrasonography could not depict any in-stent stenosis. C. Cross-sectional
contrast-enhanced ultrasonography (CEUS) image of the ICA stent shows the semi-circular soft plaque (arrow) and the remaining perfused
lumen of the ICA stent. According to the criteria of an area stenosis, the degree of the in-stent stenosis will be about 40%-50%. D. CEUS
shows some soft plaques (arrow) at the anterior ICA stent wall.

292 Ultrasonography 35(4), October 2016 [Link]

CEUS in vascular diseases

be caused by inflammatory processes and neovascularization inside Surgical intervention is recommended at any diameter greater than
the plaque; it assesses the contrast uptake in plaques via time-signal 5.5 cm in men or 5.0 cm in women [19]. The main risk is a rupture,
intensity curves (Fig. 5) [52,81-84]. with a risk of less than 1% for aneurysms with a diameter of less
than 5.5 cm, 10% for aneurysms with a diameter between 5.5 and
Abdominal Aortic Aneurysm 7.0 cm and 33% for aneurysms with a diameter greater than 7.0 cm
[19]. With a sensitivity of 95%-98%, duplex ultrasonography is the
Abdominal Aortic Aneurysm initial imaging method of choice for the diagnosis of AAAs [85]. The
AAAs are defined as an enlargement of the abdominal aorta greater use of CEUS can help visualize the direct signs of a rupture (Fig. 6)
than 3.0 cm or greater than 50% of normal size [19]. A ruptured [86].
AAA shows a mortality rate of 85% to 90% and is the 10th
most common cause of death in men over the age of 55 [19,20]. Postinterventional Follow-up
Immediate treatment of a ruptured AAA is essential, as an untreated After EVAR of an AAA, the stent needs lifelong imaging surveillance
ruptured AAA is most likely to result in death [20]. About 85% of in order to detect complications like endoleaks, fractures, or a
all AAAs are detected below the origin of the kidney vessels [19]. progressive enlargement of the AAA [27]. After EVAR, CEUS is the

A B

C D
Fig. 4. Ultrasonography after central line placement.
A. Cross-sectional B-scan identifies a hypo-echoic structure suggesting hematoma (arrowheads) without communication between the
common carotid artery (asterisk) and the internal jugular vein (arrow). B. The hematoma does not show any perfusion (arrowhead) on
color Doppler sonogram. C, D. Contrast-enhanced sonograms of the common carotid artery demonstrate the uptake of contrast inside the
hematoma (arrowheads) as the presence of a pseudo-aneurysm after central line placement without aliasing or any overwriting artifacts.

[Link] Ultrasonography 35(4), October 2016 293

 Johannes Rübenthaler, et al.

A B
Fig. 5. Ultrasonography of an atheromatous plaque in the carotid artery.
A. B-Scan of show a significant stenosis by atheromatous plaques (arrows). B. Contrast-enhanced ultrasonography shows a
neovascularization inside the plaque (arrowhead) as a sign of plaque vulnerability.

A B

Fig. 6. Ultrasonography of an infrarenal aortic aneurysm.

A, B. B-Scan (A) and color Doppler (B) sonograms demonstrate
infra-aortic aneurysm (arrows). C. Real time-resolved 4D contrast-
enhanced ultrasonography shows the same infrarenal aortic
aneurysm in the x-plane (right top), y-plane (right middle), and
z-plane (right bottom) with a volume image (left).
C

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CEUS in vascular diseases

imaging modality of choice, as it allows a fast and noninvasive as a rupture in the layer of the wall of an artery that does not
diagnosis during follow-up. The sensitivity and specificity for the occlude after puncture. The leaking blood causes a pulsatile
detection of endoleaks is 98%-100% and 82%-93%, respectively hematoma that forms a blood-filled cavity that is fed through a
(Fig. 7) [21]. connection between the cavity and the punctured artery. With
increasing size there is an increased risk for rupture, making a rapid
Vascular Complications after Transfemoral diagnosis essential [90]. Duplex ultrasonography and CEUS are the
Puncture imaging modalities of choice for the detection of pseudoaneurysms,
with CEUS being the preferred imaging technique because it is
Pseudoaneurysms independent of aliasing or overwriting artifacts (Fig. 8) [91].
False aneurysms or pseudoaneurysms after transfemoral puncture
occur in 0.05%-9% of all cases [29,87-89]. They are characterized

A B C
Fig. 7. Ultrasonography of the abdominal aortic aneurysm after endovascular aneurysm repair.
A, B. Cross-sectional B-scan (A) and color Doppler (B) sonograms show aortic aneurysm (crosshairs) with right and left stent graft legs (arrows).
No endoleak was detected. C. Contrast-enhanced ultrasonography shows a type II endoleak (arrowheads) over the left lumbar artery.

A B C
Fig. 8. Ultrasonography of the femoral artery after catheter intervention.
A, B. Cross-sectional B-scan (A) and color Doppler (B) sonograms of femoral artery (asterisks) delineate a pseudoaneurysm (arrowheads)
without any discernable flow signal. C. Contrast-enhanced ultrasonography shows a partial perfusion (arrow) of pseudoaneurysm, while the
distal part does not show any perfusion (arrowheads).

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 Johannes Rübenthaler, et al.

Arteriovenous Fistula the intervention of choice in many cases. In some cases, the
Arteriovenous fistulae occur in 0.1%-3.6% of all cases after arteriovenous fistula occludes spontaneously or can be compressed
transfemoral puncture [29,34,88]. They are described as via ultrasonography [76]. Duplex ultrasonography and CEUS are
iatrogenically abnormally connected arteries and veins. If the fistula the imaging modalities of choice for the detection of arteriovenous
is large enough, they can be hemodynamically relevant, causing fistulae, with CEUS being the superior imaging technique because
a decrease in peripheral resistance [92]. Arteriovenous fistulae of its independence from aliasing or overwriting artifacts (Fig. 9)
show a tendency to increase in size, making surgical treatment [5,77,78].

A B C
Fig. 9. Ultrasonography of the femoral artery after catheter intervention.
A, B. On cross-sectional B-scan (A) and color Doppler (B) sonograms, arteriovenous fistula with turbulent blood flow in the arteriovenous
fistula track (arrowheads) is depicted between the common femoral artery (arrow) and vein (asterisk). The complete extent of the fistulous
track is due to aliasing demarcated. C. Contrast-enhanced ultrasonography of the common femoral artery and vein identified the complete
extent of the arteriovenous fistulous track (arrowheads) and confirmed the presence of an arteriovenous communication without aliasing
or any overwriting artifacts. The distal part of the common femoral vein (asterisk) does not show any contrast uptake due to the arterial
scanning.

A B C
Fig. 10. Ultrasonography of common femoral artery dissection.
A, B. B-Scan (A) and color Doppler (B) sonograms show the common femoral artery with intimal dissection (arrowheads). Both lumens are
perfused in the color Doppler setting (arrows). C. Due to its superior spatial resolution, the dissection membrane (arrowheads) and both
perfused lumens are clearly depicted on contrast-enhanced ultrasonography.

296 Ultrasonography 35(4), October 2016 [Link]

CEUS in vascular diseases

Dissection puncture [29,66,94] and are a rather common complication in this

Dissections occur in 0.3%-3.6% of all cases after transfemoral circumstance. Normally, hematomas are locally limited and are
puncture [66,93]. Similarly as was described before for the resorbed within a short period of time. They can be easily depicted
dissection of the carotid arteries, vascular ultrasonography is the using duplex ultrasonography.
imaging modality of choice for the detection and characterization
of dissection, by showing the mural hematoma as well as the false Conclusion
and true lumen, and by additionally visualizing any decreased blood
volume flow in the false lumen that results in an increased risk for For the detection, characterization, and follow-up of vascular
thrombosis, embolization, or even partial or total occlusion of the pathologies, duplex ultrasonography is the first choice. However,
artery [69-71]. As discussed before, modern ultrasound probes duplex ultrasonography has technical limitations in diagnostic use,
can identify small dissection with very thin membranes of less than for example, due to aliasing artifacts that can complicate diagnosis.
1 mm [4,72,73]. CEUS can help aid diagnosis and improves the The use of CEUS can increase the diagnostic performance in
diagnostic accuracy in difficult cases (Figs. 10, 11) [51,53]. difficult vascular disorders compared to duplex ultrasonography.
Thus, CEUS has become a promising, safe, noninvasive imaging
Hematoma tool in different aortic pathologies, particularly for the detection of
Hematomas occur in 0.4%-11% of all cases after transfemoral endoleaks following endovascular treatment of AAAs. Examinations

A B

C D
Fig. 11. Ultrasonography of the common femoral artery with suspicious dissection.
A, B. B-Scan (A) and color Doppler (B) sonograms show incomplete perfusion of the vessel lumen (arrows). C, D. Longitudinal (C) and cross-
sectional (D) contrast-enhanced images demonstrate a floating embolus (arrowheads) in the center of the common femoral artery (arrow).
Due to its superior spatial resolution, contrast-enhanced ultrasonography could be used to exclude the possibility of arterial dissection.

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 Johannes Rübenthaler, et al.

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