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Review
. 2017 Feb 9;20(2):97-109.
doi: 10.1007/s40477-017-0239-4. eCollection 2017 Jun.

Contrast-enhanced ultrasound of the carotid system: a review of the current literature

Vasileios Rafailidis  1 , Afroditi Charitanti  1 , Thomas Tegos  2 , Evangelos Destanis  1 , Ioannis Chryssogonidis  1
Affiliations
Review

Contrast-enhanced ultrasound of the carotid system: a review of the current literature

Vasileios Rafailidis et al. J Ultrasound. .

Abstract
in English, Italian

Carotid disease is a major current health problem accounting for a significant part of stroke patients. Ultrasound with colour Doppler and spectral analysis is the primary imaging technique used for screening and diagnostic evaluation of the extracranial part of carotid arteries offering identification and grading of carotid disease. However, inherent limitations of this technique include flow-related artefacts like Doppler angle dependence and aliasing artefact which may sometimes hinder complete assessment of a stenotic part of the vessel, potentially failing to address clinically significant differential diagnosis issues. The intravenous use of microbubbles as an US contrast agent has been introduced for the supplementation of conventional technique. The value of contrast-enhanced ultrasound (CEUS) has been investigated in the evaluation of carotid disease leading to promising results. CEUS provides improved flow visualization free of artefacts and detailed plaque surface delineation, thus being able to accurately grade stenosis, identify carotid plaque ulcerations, differentiate occlusion from highly stenotic plaques and identify carotid dissection. Furthermore, microbubbles can be used to identify and grade intraplaque neovascularization, carotid wall inflammation in patients with arteritis, follow-up patients after carotid intervention and assist interventional procedures reducing the need for nephrotoxic contrast agents. The purpose of this review is to present and discuss the current literature regarding the various uses of CEUS in carotid arteries.

La malattia carotidea rappresenta un grosso problema attuale di una parte significativa dei pazienti con ictus. L’ecografia con color Doppler e l’analisi spettrale è la metodica di imagine di prima istanza utilizzata per lo screening e la valutazione diagnostica della parte extracraniale delle arterie carotidee che offre l’identificazione e la classificazione della malattia carotidea. Tuttavia le limitazioni intrinseche di questa tecnica includono gli artefatti connessi al flusso, come dipendenza dall’angolo Doppler e l’artefatto aliasing che talvolta possono ostacolare la valutazione totale di una parte stenotica del vaso, avendo ad affrontare potenzialmente significativi problemi clinici di diagnosi differenziale. L’ uso endovenoso di microbolle come agente di contrasto nell’ecografia è stato introdotto per la supplementazione della tecnica convenzionale. Il valore del mezzo di contrasto nell’ ecografia (CEUS) è stato studiato per la valutazione della patologia carotidea e sta portando risultati promettenti. CEUS offre una migliore visualizzazione dettagliatta, libera da artefatti di flusso della placca e la delineazione della superficie essendo così in grado di precisare il grado di stenosi ed identificare ulzerazioni della placca carotidea, differenziare l’occlusione dalle placche altamente stenotiche e identificare la dissezione carotidea. Inoltre, le microbolle possono essere utilizzate per l’identificazione del grado di neovascolarizzazione intraplacca, l’infiammazione della parete carotidea in pazienti con l’arterite, di eseguire il follow-up dei pazienti dopo l’intervento carotideo e assistere le procedure interventistiche riducendo la necessità di mezzi di contrasto nefrotossici. Lo scopo di questa rassegna è quello di presentare e discutere la letteratura attuale per quando riguarda i vari usi di CEUS nelle arterie carotidee.

Keywords: Atherosclerosis; Carotid; Contrast-enhanced ultrasound; Occlusion; Plaque; Stenosis.

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Conflict of interest statement

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Figures

Fig. 1
Fig. 1
A 70-year-old asymptomatic male patient with a smooth anechogenic carotid plaque. Colour Doppler imaging a shows significant elongated narrowing of the internal carotid artery lumen raising suspicion of an elongated stenosis. CEUS b revealed the presence of a focal smooth carotid plaque, accurately delineating its surface. MDCTA c confirmed CEUS findings
Fig. 2
Fig. 2
A 77-year-old asymptomatic male patient with ulcerated carotid plaque. Colour Doppler imaging a identifying a highly stenotic plaque with relatively irregular surface, which however could not be accurately delineated. Long-axis CEUS image b revealing the presence of a type 3 ulcer (arrowhead). Short-axis CEUS image c confirming the ulcer’s presence (arrowhead). MDCTA d confirmed the presence of a highly stenotic and ulcerated carotid plaque (arrowhead)
Fig. 3
Fig. 3
A 66-year-old asymptomatic male patient with an irregular internal carotid artery plaque. Colour Doppler imaging a detected atherosclerotic changes in the origin of the internal carotid artery with absence of blood flow signals distally, raising suspicion of occlusion. CEUS b revealed the presence of flow within a highly stenotic and irregular plaque. MDCTA c was in concordance with CEUS findings
Fig. 4
Fig. 4
A 50-year-old female patient with stroke and carotid occlusion. Colour Doppler imaging a showed absence of colour flow signals within the internal carotid artery suggesting total occlusion. CEUS b confirmed the absence of flow in the internal carotid artery establishing the diagnosis of total occlusion. MDCTA c confirming the diagnosis
Fig. 5
Fig. 5
A 65-year-old male patient referred for follow-up after carotid stenting. Colour Doppler imaging a confirmed the stent’s patency although the stent’s lumen was not completely filled, potentially due to restenosis. CEUS b proved complete filling of the stent with moving microbubbles, excluding the possibility of restenosis
Fig. 6
Fig. 6
A 77-year-old male patient with a carotid plaque showing intraplaque neovascularization on CEUS. Early CEUS image a shows moving microbubbles filling the vascular lumen and delineating a hypoechoic plaque. Delayed CEUS image b showing no enhancement of the lumen while moving microbubbles can be seen within linear structures inside the plaque, representing neovascularization (arrowhead). Immunohistochemical examination c of the resected plaque with CD34 staining demonstrated the presence of intraplaque neovascularization under the plaque’s fibrous cap (×10)
Fig. 7
Fig. 7
A 62-year-old male patient with internal carotid artery dissection. Colour Doppler imaging a showing flow reversal in common carotid artery and no blood flow signals within the internal carotid artery raising suspicion of total occlusion. CEUS image b revealed the presence of blood flow distally to the point of suspected occlusion by colour Doppler (a) and identifying a free-floating anechoic and non-enhancing membrane within the lumen, which could potentially represent an intimal flap (arrowhead). MDCTA c confirmed the presence of an intimal flap in combination with an elongated intramural haematoma
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