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 Table of Contents  
Year : 2018  |  Volume : 28  |  Issue : 4  |  Page : 218-227

Three-dimensional echographic evaluation of carotid artery disease

1 Department of Medical Surgical, Molecular and Critical Area Pathology; Department of Cardiac, Thoracic and Vascular, Pisa University, Pisa, Italy
2 Department of Clinical and Experimental Medicine, Pisa University, Pisa, Italy
3 Department of Translational Research and New Technologies in Medicine and Surgery, Pisa University, Pisa, Italy

Date of Web Publication24-Dec-2018

Correspondence Address:
Nicola Riccardo Pugliese
Department of Cardiac, Thoracic and Vascular, Azienda Ospedaliero-Universitaria Pisana, Via Paradisa, Pisa 256124
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jcecho.jcecho_57_18

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The introduction of three-dimensional echography (3D echo) in vascular field is not recent, but it still remains a seldom-used technique because of the costs of ultrasound probe and the need of dedicated laboratories. Therefore, despite significant prognostic implications, the high diagnostic accuracy in plaque definition, and the relative ease of use, 3D echo in vascular field is a niche technique. The purpose of this review is mainly clinical and intends to demonstrate the potential strength of a 3D approach, including technical aspects, in order to present to clinicians and imagers the appealing aspects of a noninvasive and radiation-free methodology with relevant diagnostic and prognostic correlates in the assessment of carotid atherosclerosis. A comprehensive literature search (since 1990s to date) using the PubMed, MEDLINE, and Cochrane libraries databases has been conducted. Articles written in English have been assessed, including reviews, clinical trials, meta-analyses, and interventional/observational studies. Manual cross-referencing was also performed, and relevant references from selected articles were reviewed. The search was limited to studies conducted in humans. Search terms, retrieved also with PubMed Advanced search and AND/OR Boolean operators (mainly in title and abstract), included three-dimensional, echo, stroke/transient ischemic attack, predictors, carotid, imaging, and biomarkers.

Keywords: Carotid atherosclerosis, color Doppler ultrasound, internal carotid artery stenosis, three-dimensional ultrasound imaging, total plaque volume

How to cite this article:
Calogero E, Fabiani I, Pugliese NR, Santini V, Ghiadoni L, Di Stefano R, Galetta F, Sartucci F, Penno G, Berchiolli R, Ferrari M, Cioni D, Napoli V, De Caterina R, Di Bello V, Caramella D. Three-dimensional echographic evaluation of carotid artery disease. J Cardiovasc Echography 2018;28:218-27

How to cite this URL:
Calogero E, Fabiani I, Pugliese NR, Santini V, Ghiadoni L, Di Stefano R, Galetta F, Sartucci F, Penno G, Berchiolli R, Ferrari M, Cioni D, Napoli V, De Caterina R, Di Bello V, Caramella D. Three-dimensional echographic evaluation of carotid artery disease. J Cardiovasc Echography [serial online] 2018 [cited 2020 Sep 18];28:218-27. Available from: http://www.jcecho.org/text.asp?2018/28/4/218/248414

  Introduction Top

Approximately 20%–30% of ischemic strokes are caused by the rupture of carotid artery plaques, and the percentage diameter reduction in the carotid arteries is used as an indicator for stroke risk.[1],[2] The risk factors leading to plaque rupture, however, remain incompletely understood. Stroke rates achieved after guideline-directed carotid endarterectomy (CEA) for high-grade carotid stenosis in symptomatic patients (stroke/transient ischemic attack [TIA]) are significantly lower than those observed with best medical therapy alone; at the same time, in asymptomatic patients, the majority of medically treated patients remain stroke free during follow-up.[3] Moreover, in asymptomatic population, increasing degrees of stenosis have not been associated with a correspondingly increased risk for stroke/TIA.[4] It is, therefore, important to identify additional markers to assess the risk of stroke and to identify patients who would benefit most from revascularization.[5]

Magnetic resonance imaging (MRI) is a sensitive and specific method for determining the plaque characteristics.[6],[7] At present, computed tomography angiography is not much accurate in delineating plaque composition. It is, however, useful to identify the luminal surface outline.[8],[9] Duplex ultrasonography (DUS) is the most widely available and low-risk noninvasive test to assess carotid plaque severity, although its correlation with angiographically measured stenosis severity is low.[10] Two-dimensional (2D) B-mode imaging can visualize a number of anatomic features of the arterial wall and plaque. An important strength of ultrasonography is its ability to provide real-time physiologic information on blood flow (Doppler methods). While the image quality of ultrasound and the observable anatomic detail continues to improve, it is still limited by interobserver variability. The addition of three-dimensional (3D) imaging protocols has attempted to address that limitation.[11]

The noninvasive morphologic features of pre-embolic unstable plaques and their correlation with stroke still remain ill defined, due to a low incidence of stroke in asymptomatic patients with carotid plaques. Therefore, there continues to be a need to develop and validate plaque features that will identify patients at risk for future plaque disruption and athero-embolic cerebral infarction. In the past three decades, there has been a significant increase in the use of 3D carotid ultrasound for estimating the carotid plaque burden (CPB) through the estimation of luminal cross-sectional area.

The purpose of this review is mainly clinical and intends to demonstrate the potential strength of a 3D approach, including technical aspects, in order to present to clinicians and imagers the appealing aspects of a noninvasive and radiation-free methodology with relevant diagnostic and prognostic correlates in the assessment of carotid atherosclerosis.

  Searching Strategy Top

A comprehensive literature search (since 1990s to date) using the PubMed, MEDLINE, and Cochrane libraries databases has been conducted. Articles written in English have been assessed, including reviews, clinical trials, meta-analyses, and interventional/observational studies. Manual cross-referencing was also performed, and relevant references from selected articles were reviewed. The search was limited to studies conducted in humans. Search terms, retrieved also with PubMed Advanced search and AND/OR Boolean operators (mainly in title/abstract), included three-dimensional, echo, stroke/TIA, predictors, carotid, imaging, and biomarkers.

  History Top

From an historical perspective, in 1994, a volumetric method was introduced to assess plaque burden [Table 1].[12] Initial evaluations of carotid plaque volume were difficult; the disk segmentation method required collection of a set of 2D cross-sectional slices captured by moving the ultrasound probe on the neck along the carotid artery with a mechanical device. The plaque area was traced using continuous cross sections of the artery, stepping through the plaque at intervals of approximately 1 mm, and the slices were summed to calculate the plaque volume. Early work specified the inter slice distance, reliability, reproducibility, and other technical details.[13],[14],[15],[16],[17] Ludwig et al.[18] in 2008 and following articles in 2014[19],[20] and 2015[21],[22] underlined good reproducibility and also discovered that reproducibility was superior for big plaques than for thin ones. The disk segmentation method was not only difficult, but also required 2–3 months of preparation. Initial semi-automated techniques[23],[24] reduced the number of slices of the plaque that needed manual input to establish the proximal and distal ends of each plaque. The operator had to delineate slices at the midpoint, 25% and 75% of the length of the plaque, with automated interpolation of the surface of the rest of the plaque. In 2013, an automatic technique was developed using mechanical movement of the probe along the artery[25] that offered good agreement with manual segmentation by experts. However, the mechanism used to move the ultrasound probe is big and clumsy, and it is difficult to use in overweight patients and in patients with small necks. A mechanical sweep, acquired by keeping the probe in one site and having the angle changed mechanically, is quicker and more suitable. Recently, Græbe et al.[21] showed that the mechanical sweep gave enhanced reproducibility of plaque volume determination compared with the manual movement of the probe along the artery.
Table 1: Quantification of atherosclerotic plaques in carotid arteries by three-dimensional ultrasound

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  Three-Dimensional Ultrasonography: A Clinical Stand-Point Top

From a clinical stand-point, the introduction of 3D imaging in the field of carotid ultrasounds stems at least from the following three main concepts:

  1. The recognition of plaque pathophysiology, morphology, and its progression [Figure 1] and [Figure 2]
  2. The importance of a direct evaluation of arteries (especially carotid) and tight follow-up besides the simple assessment of conventional risk factors, suggesting an “arterial target-based” instead of risk factor-based approach in cardiovascular (CV) preventive strategies
  3. The inherent limitations in intimal media thickness (IMT) assessment and the potential implications for risk stratification reassessment (plaque burden).
Figure 1: Three-dimensional vascular probe-automated mechanical sweep echographic probe

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Figure 2: Vascular Plaque Quantification Software Offline (PACS) advanced analysis for total plaque volume and maximum percentage area reduction definition

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Paired with the technological advances in 3D reconstruction and validation (i.e., magnetic resonance angiography [MRA]), together with an important reassessment of Doppler methodology, 3D carotid ultrasound is expected to contribute to the re-evaluation of the entire construct of the atherosclerotic process behind stroke/TIA and CV risk stratification.

  Total Plaque Volume and Prognosis/Risk Stratification Top

Atherosclerotic plaque is a 3D phenomenon that is irregular in shape, and measurements performed solely in a 2D plane may miss the true extent of the plaque if it is out of plane. Compared with 2D imaging, 3D quantification of carotid plaque was shown to be more sensitive for clinically important angiographic stenosis in symptomatic patients. Plaques progress along the vessel is 2.4 times faster than the thickening of the wall.[26] Therefore, methods that capture both longitudinal and circumferential growths (i.e., area and volume) are inherently more sensitive than methods limited to thickness measurements (i.e., diameter-reducing stenosis). The 5-year risk of stroke, myocardial infarction (MI), and vascular death is 19% for plaques with a longitudinal sectional area of 1.2–6.7 cm2 compared to 6% for areas of 0–0.1 cm2. Therefore, plaque area and volume (rather than diameter-reducing stenosis) may be better predictors of future rupture.

After adjusting for age, cholesterol, blood pressure, sex, homocysteine, smoking, diabetes, and treatment of cholesterol and blood pressure, patients in the top quartile of total plaque area (TPA) had a three times higher 5-year risk of death, stroke, or MI.[27],[28] In each quartile of TPA, the 5-year risks were approximately 5%, 10%, 15%, and 20%. Therefore, TPA was better than the Framingham risk profile in predicting risk. During the 1st year of follow-up, almost half of the patients had plaque progression, a quarter had retrogression, and a quarter was constant. Those with plaque development had twice the risk of events, after adjustment for the group of risk factors listed before. TPA significantly improves risk prediction[28] when added to risk calculation using scores based on risk factors [Table 2].
Table 2: Three-dimensional ultrasound-based carotid plaque quantification: Vascular event risk prediction

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AlMuhanna et al. investigated the variability, reliability, and the least amount of change detectable by one-dimensional plaque measures, as well as 2D and 3D measures of plaque morphometry, that can be applied in a clinical environment in patients with carotid stenosis.[22] They found carotid plaque diameter measurements from B-mode images as they have a high variability while plaque burden resulted readily and reliably measurable with a 3D US technique using a clinical scanner.

In 2011, Makris et al.[1] performed a systematic review of seven studies on the reproducibility of plaque volume reported an overall good intra- and inter-observer reproducibility. In addition, in ten further studies evaluating 3D plaque progression, volume performed better than IMT for plaque assessment in response to therapy [Table 3].
Table 3: Reproducibility of three-dimensional ultrasound

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Importantly, the time taken to complete the quantification was not longer than 10–15 min. These developments increase the possibility for 3D quantification of carotid plaques to reach the clinical environment. It reliably detects plaque volume changes as low as 4%–6% with 95% confidence.[29] Wannarong measured TPA, total plaque volume (TPV), and IMT with 3D ultrasound in 349 patients and followed the patients annually for 5 years. Using Cox regression analysis, survival free of any CV events (stroke, vascular death, TIA, or MI) was predicted by TPV progression or regression. TPA was a predictor of stroke, death, and TIA, but not of CV events. Progression or regression of IMT thickness did not predict any of these events.[1]

Carotid 3D plaque volume is also more sensitive to the effects of therapy than coronary intravascular ultrasound (IVUS), whereas carotid plaques are focal and can change in three dimensions; coronary plaques are present along the entire length and entire circumference of the artery, so change is reduced to a change in average thickness.

A study on the effects of statins on plaque progression/regression indicates that change in TPA or TPV can be observed after 3 months.[30]

Sillesen et al.[26] in 2012 studied 6101 asymptomatic patients without known CV disease with a 3D-based ultrasound approach (plaque burden), comparing CPB, carotid intima-media thickness (cIMT), ankle–brachial index (ABI), and abdominal aortic diameter (AAD) to coronary artery calcium score (CACS). In 3D, more than half of the patients had intermediate Framingham Risk Score (6%–20% 10-year risk). Carotid plaques were identified in 78% of cases and abnormal ABI in 10%; CPB demonstrated a higher correlation with CACS than did cIMT, AAD, and ABI.

Johri et al.[31] performed 2D and 3D carotid ultrasound scans on seventy consecutive patients referred for coronary angiography on the same day for plaque quantification in the carotid bulbs. 3D carotid ultrasound resulted in a higher negative predictive value and sensitivity relative to 2D carotid ultrasound and accurately predicted the absence of significant CAD.

Subsequently, in the BioImage Study (A Clinical Study of Burden of Atherosclerotic Disease in an At-Risk Population), the authors validated this approach in order to identify imaging biomarkers that predicted near-term (3-year) atherothrombotic events.[26] Bilateral carotid artery plaque areas were summed to obtain a CPB. Over a median follow-up of 2.70 years, after correction for risk factors and matching with individuals without any CPB, hazard ratios for MACE were 0.780 (95% confidence interval [CI]: 0.31–1.91), 1.45 (95% CI: 0.670–3.140), and 2.36 (95% CI: 1.13–4.92) in increasing CPB tertiles with comparable results for CACS. Net reclassification improvement appreciably improved with either CPB (0.23) or CACS (0.25). MACE rates increased concurrently with higher levels of both CPB and CACS, thus showing that subclinical carotid or coronary atherosclerosis actually increases risk predictions and reclassification compared with traditional risk factors, with similar results for either modality.

  Vessel Wall Volume Top

In patients without plaque, such as children and healthy volunteers, sometimes it has been a common practice to measure IMT. However, a viable alternative is the measurement of vessel wall volume (VWV, i.e., the volume of the artery minus the volume of the lumen).[32] That measurement, which is conceptually equivalent to a 3D IMT, has significant advantages over IMT. First, like TPV,[33] VWV has a much greater dynamic range; thus, it also potentially reduces sample size and duration of therapy compared with IMT and IVUS. Atorvastatin significantly reduced VWV in 3 months[34] in the same patients in which TPV was measured in the study discussed previously.[35] Dietary weight loss, probably through reduction of blood pressure, significantly reduced VWV in 2 years.[36]

  Ulceration, Echolucency, and Plaque Texture: Approaching Plaque Composition Top

An additional advantage of 3D imaging is an improved ability to evaluate the plaque surface. Ulceration, as detected by surface irregularity, is an important indicator of plaque instability, as it is strongly associated with the presence of rupture, plaque hemorrhage, large lipid core, less fibrous tissue, and overall instability.[37] Angiographic studies of carotid arteries have shown that patients exhibiting ulceration and high stenosis (85%) are twice as likely to have a stroke than patients who did not have ulcers;[38] likewise, patients with carotid plaque surface irregularities are more likely to have a history of MI and to develop fatal acute MI, nonstroke vascular disorders, and sudden cardiac deaths than patients with smooth plaque.[39] However, the accuracy of detecting ulceration by angiography is relatively low, with high rates of false positives and false negatives,[40] and B-mode ultrasound has been found to be a more accurate method for ulcer detection.[41]

Kuk et al.[19] quantified carotid global ulcer volume by 3D ultrasound to analyze the relationship of total ulcer volume to vascular events (MI, death because of CV reasons, strokes, TIA, revascularization, or death because of CV reasons). Ulcer volume was defined as a clear discontinuity in an atherosclerotic lesion, with a volume ≥1 mm3 as measured using traditional manual segmentation. The sum of the volumes of any ulcers seen in both carotids was the total ulcer volume. Participants were monitored for a 5-year follow-up. Participants with global ulcer volume ≥5 mm3 had a considerably greater risk of experiencing stroke, TIA, or death and non mi torna! the combined endpoint, including MI-related death and revascularization. Smaller ulcer volumes predict neither events nor ulcer depth.

Madani et al. recognized carotid ulcerations with 3D ultrasound in asymptomatic patients with carotid stenosis >60%. These authors also performed transcranial Doppler (TCD) to detect micro-embolization to the middle cerebral artery. Patients with ≥3 ulcers were more likely to have a stroke or death during a 3-year follow-up (18% vs. 2%). Furthermore, patients in whom TCD detected micro-emboli also had an elevated risk of stroke or death (20% vs. 2%).[42]

3D ultrasound is superior to 2D ultrasound in allowing the differentiation between ulceration and gaps between consecutive plaques adjacent to one another.[43] 3D ultrasound has been used to detect changes in the morphology of ulcers by comparing the 3D surface features of ulcerated plaque:[44] the identification and quantification of ulcers by 3D ultrasound in association with carotid stenosis (60%) has demonstrated a correlation between the number of ulcers (three or more) and the risk of stroke or death.[45] Computer-assisted methods for the analysis of ultrasound imaging are constantly evolving for achieving greater accuracy in plaque quantitative analysis. Chiu et al.[46] demonstrated that mean and Gaussian curvatures can be used to identify ulcers from in vivo 3D ultrasound images; the algorithm was validated using synthetic surfaces and vascular phantoms containing “ulcers” that were 2–4 mm in diameter. In 124 patients, the total ulcer volume was found to be predictive of a higher risk for CVD events.[40] Quantification of plaque volume and ulceration can be conducted with most commercially available software, but there is currently no standard procedure for measuring ulceration by either 2D or 3D ultrasound, and as suggested by Muraki et al.,[47] current classification criteria may be too conservative for accurate ulcer detection. It has long been thought that echolucent plaque represented “soft plaque” that was more likely to rupture and embolize. Several studies have shown that echolucency predicted higher risk of CV events.[48],[49],[50] More recently, radiofrequency analysis (as opposed to gray-scale analysis) has been used to study plaque “texture,” a way of assessing plaque composition.[51],[52] Inhomogeneity of plaque texture and some other features of plaque texture have been shown to identify patients at higher risk of events.[53],[54] Noninvasive characterization of intraplaque hemorrhage and enlarging lipid cores may identify individuals at risk for stroke. 2D longitudinal sectional B-mode images have been used to predict plaque histology, but a single slice provides limited information. Tissue characterization from 3D ultrasound may offer more comprehensive information. This approach may improve risk stratification, monitoring for the effectiveness of pharmacologic management, and selection of patients for carotid revascularization.[42]

Van Engelen et al. examined carotid ultrasound plaque texture and its changes in 298 patients at risk of events and compared them with the measurements of plaque volume and other risk factors as predictors of vascular events during 1 year. Patients were followed up to 5 years for MI, TIA, and stroke. In multivariate Cox regression analysis, changes in plaque texture and TPV were both significant predictors, whereas the Framingham risk score was not.[20]

  Performance of Three-Dimensional Versus other Methodologies (Angiography and Magnetic Resonance Imaging) Top

Yao et al. studied 14 patients both with 3D ultrasound and carotid angiography (CA). A 3D ultrasound examination was performed also after surgery. The volume and length of twenty randomly selected lesions were measured from 3D data sets. The severity of stenosis was measured by 3D ultrasound using both the area and the diameter of several cross-sectional examinations at the most stenotic location; the results were then compared with CA, showing good correlation with 3D ultrasound in the quantitative analysis of carotid stenosis.[20]

In another article,[55] the degree of luminal narrowing, measured as percentage area reduction in the 3D data set, correlated well with the degree of stenosis estimated by CA. In particular, 3D ultrasound showed good sensitivity and diagnostic accuracy for the detection of significant stenosis of extracranial carotid artery, showing, for stenosis between 40% and 70%, a higher degree than CA.

In 2014, Pelz et al.[56] performed 3D ultrasound of carotid vessels including 3D ultrasound quantification of internal carotid artery (ICA) stenosis and contrast-enhanced-MRA (CE-MRA) of the neck vessels, showing good interrater and intermethod agreement in comparison to CE-MRA.

Chiu et al.[46] developed an accurate surface-based 3D iterative closest point registration method to align surfaces reconstructed from outer wall boundaries segmented from 3D ultrasound and MRIs. The 3D ultrasound image was transformed according to the registration result and re-sliced to match the corresponding 2D transverse MRIs.

Vicenzini et al.[57] described the use of this technique in conditions different than carotid stenosis, such as bifurcations and changes of the caliber or course of the neck vessels. In forty normal controls, seven patients with caliber alterations (four carotid bulb ectasia and three internal carotid lumen narrowings), 45 patients with course variations (tortuosity and kinking), and 35 patients with ICA stenosis of various degrees, they showed the feasibility and the improvement of carotid axis imaging through a better presentation of caliber variations and vessel course “at a glance.”

Igase et al.[58] evaluated the utility of 3D ultrasound for assessing carotid artery stenosis compared with MRA. In 58 patients with carotid stenosis, they showed how ultrasound imaging resulted useful in the detection of mild stenosis, ulcerated plaque, or mobile plaque in comparison with MRA.

  Three-Dimensional Doppler Top

DUS has numerous pitfalls when the quantification of stenosis is attempted by spectral blood velocity parameters.[59],[60],[61] In particular, for stenosis within the low (<50%) to moderate (50%–70%) range, intrastenotic velocity increases only slowly relative to the luminal loss, thereby resulting in a lack of diagnostic accuracy, that often requires additional morphological estimation of plaque stenosis in B-mode or color Doppler images, according to the North American Symptomatic Carotid Endarterectomy Trial method.[60],[61],[62],[63],[64] Direct measurement of stenotic lumen reduction using 2D color Doppler ultrasound images delivered inconsistent results and may not improve accuracy when this method is used alone.[62],[63]

Wessels et al.[65] evaluated the intermethod agreement of ICA stenosis using digital subtraction angiography (DSA) compared with 3D ultrasound in 49 patients. Patients were investigated with a color Doppler system using the power mode. 3D ultrasound slightly underestimated the mean stenotic degree. The intermethod agreement comparing DSA with 3D echo was analyzed with the Bland and Altman test, which showed good agreement, yielding higher accuracy than CDS alone.

Stenosis grading with 3D echo using a dedicated volume probe generating static 3D images for immediate online and posthoc offline multiplanar rendering of relevant vessel segments, which is an innovative approach. The static 3D color Doppler images can be acquired after a quick topo-anatomic orientation with real-time four-dimensionally guided gray-scale imaging using the same probe.[59]

  Conclusions Top

3D carotid ultrasound is an accurate and readily available method for atherosclerosis monitoring. It allows a fast and reproducible, volumetric, quantification of disease, consistent with a better risk stratification of individuals, without a significant slowdown of lab workflow. Validated against DSA and MRI, with the additional values of wall definition, plaque texture evaluation, and color Doppler all in one technique, it may provide a significant aid for redefinition of treatments in primary and secondary prevention, guiding different follow-up strategies.


We would like to thank Vassiliki Avramopoulou for her editorial assistance and English revision.

Financial support and sponsorship

The review is part of a project financed with Pisa University - PRA (Progetto di Ricerca di Ateneo) 2017 public fundings.

Conflicts of interest

There are no conflicts of interest.

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  [Table 1], [Table 2], [Table 3]

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