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Perspectives in Medicine (2012) 1, 108111

Bartels E, Bartels S, Poppert H (Editors):

New Trends in Neurosonology and Cerebral Hemodynamics an Update.
Perspectives in Medicine (2012) 1, 108111

journal homepage:

Early ultrasound imaging of carotid arteries in the

acute ischemic cerebrovascular patients
Maria Fabrizia Giannoni a,, Edoardo Vicenzini c, Enrico Sbarigia b,
Vittorio Di Piero c, Gian Luigi Lenzi c, Francesco Speziale b

Dept Paride Stefanini, Vascular Ultrasound Investigations Unit, Sapienza University of Rome, Italy
Dept Paride Stefanini Vascular Surgery, Italy
Dept Neurological Sciences, Sapienza, University of Rome, Italy

Acute cerebral Background and purpose: The early identication of ischemic stroke pathophysiology may lead
ischemia; to different diagnostic and therapeutical strategies. In 1/3 of patients, stroke is related to
Unstable carotid carotid disease, when a vulnerable plaque evolves with surface rupture and local apposition of
plaques; highly embolic/thrombotic material. This being a rapidly evolving dynamic process, the value of
Ultrasonography; its early identication may be underestimated. With the diffusion of high-resolution ultrasound
Contrast enhanced equipments, the possibility of identifying these features of plaque vulnerability has become
ultrasound; easily available. These plaque characteristics have to be always considered in the patient man-
Carotid surgery; agement, in order to avoid further worsening of neurological conditions or to prevent recurrent
Timing of carotid events, and to choose the appropriate strategies.
surgery Methods: Early ultrasonography was performed with high frequency probes (9, 15, 18 MHz) in
patients admitted to emergency area for acute ischemic symptomatology from carotid stenosis.
Results: In 8 patients admitted to the emergency area few hours after the onset of neurologi-
cal symptoms, we detected peculiar plaque characteristics closely related to the neurological
events and at high risk of further embolic events with local thrombosis, surface plaque rupture
and carotid oating thrombi. All these cases were successfully submitted to emergency carotid
endarterectomy repair.
Conclusions: Timing of carotid endarterectomy has always been debated in stroke patients
clinical management, depending on several factors. All imaging techniques contribute to the
identication of plaque morphology features, but early admission of stroke patients to the emer-
gency areas and early US have a crucial leading role in detecting plaque rupture and dynamic
changes in real-time. Peculiar characteristics of high unstable plaques allow the identication
of those lesions at particularly high risk of further embolic events according to their fragile
characteristics that may benet from early surgery.
2012 Elsevier GmbH. Open access under CC BY-NC-ND license.

Corresponding author at: Dept Paride Stefanini, Vascular Ultrasound Investigation Unit, Vascular Surgery, Policlinico

Umberto I, Viale del Policlinico 155 00161 Rome, Italy. Tel.: +39 6 49970660; fax: +39 49970652.
E-mail address: (M.F. Giannoni).

2211-968X 2012 Elsevier GmbH. Open access under CC BY-NC-ND license.

Early ultrasound imaging of carotid arteries in the acute ischemic cerebrovascular patients 109

Introduction of further embolic events, as mobile thrombus over plaque

Vulnerable atherosclerotic plaque rupture with surface Symptoms included: hemiparesis (n = 5), amaurosis fugax
apposition of thrombotic material is the predominant (n = 3), language impairment (n = 3). Three patients had a
pathological substrate of acute cerebrovascular events, combination of the symptoms.
accounting for 30% of all strokes [1]. In acute ischemic stroke Mean NIHSS on admission was 4 (min: 0, max: 8). Cere-
patients, in addition to standard imaging techniques aimed bral Magnetic Resonance Imaging with diffusion-weighted
at the decision whether to perform thrombolysis, early sequences documented the presence of ischemic areas in
ultrasound investigation is fundamental to detect potential 7 patients in the corresponding omolateral carotid territory.
embolic carotid source in order to avoid further emboliza- All patients presented hemodynamic internal carotid
tion by means of carotid surgery. stenosis consistent with the clinical symptoms. Hetero-
The aim of this report is to evaluate the possibility of geneous, mostly hypoechoic, complicated plaques were
early detection of these carotid plaque features with ultra- detected in all cases. Moreover, high-resolution B-Mode
sound and to discuss the implications of this diagnosis in imaging performed with high frequency probes and spatial
order to plan the most appropriate strategy in acute cere- compound to better visualize plaque surface and texture,
brovascular ischemic patients. demonstrated an extensive rupture of the surface with
structure ssurations (Fig. 1), intraoperatively conrmed.
Ultrasound B-Mode imaging also allowed the detection of
Material and methods an abnormal motion of the soft parts of the plaques,
in particular nearby the sites of plaque rupture. In two
cases, real-time B-Mode imaging demonstrated an endothe-
All patients referred to the emergency area for the onset
lial oating ap represented by the ruptured cap of the
of acute ischemic neurological symptoms were subjected
plaque, mobile in the lumen, and thus conrming the high
to Duplex Ultrasonography (DUS) (Siemens Sequoia 512 and
potential embolic risk of these lesions (Fig. 2). Mobile clots
Siemens S2000 apparatus), according to the conventional
were also visualized from the surface at the site of plaque
methodology and standard AHA and European Guidelines
rupture in two cases (Fig. 3). Contrast ultrasound imag-
with high-resolution probes (9, 15, 18 MHz), Tissue Harmon-
ing detected a high density of microvessels in the plaque
ics and Spatial Compound. DUS was performed immediately
tissue consisting with relevant neoangiogenesis, as already
after brain imaging. No patients with ipsilateral (middle
described elsewhere [2,3] in acute symptomatic plaques.
cerebral artery) occlusion or an ischemic area > 1/3 of the
Furthermore, contrast ultrasound allowed a better visu-
Middle Cerebral Artery area underwent carotid endarterec-
alization of the plaque extension and surface, better
demonstrating the rupture extended deeply from the sur-
face to the core of the plaque. In one case, a small ulceration
with a mobile clot was also identied.
Results All patients were immediately and successfully submitted
to CEA: mean NIHSS at discharge was 2 (min: 0, max: 4).
We report 8 patients (M: 6, F: 2, mean age 64.7 yrs, range
5378 yrs), referred to the emergency area for the onset Discussion
of acute neurological symptoms occurred no more than 6 h
before, in whom we detected with US immediately per- Stroke remains a leading cause of disability and death world-
formed after brain CT scan, plaque features of high risk wide [4]. About one-third of ischemic strokes arise from

Figure 1 Left side MRI: cerebral ischemic lesion. Right side: intraoperative macroscopic ndings ultrasound imaging of the ruptured
plaque with the mobile ap (Clip 1).
110 M.F. Giannoni et al.

Figure 3 Ultrasonography: hypoechoic, mobile thrombus in

the proximal part of the plaque (left side of the image) (Clip 3).

Figure 2 Ultrasonography: hypoechoic, mobile thrombus in

the distal anterior part of the plaque (right side of the image)
(Clip 2). degree of stenosis, low GSM and surface ulceration are
important predictors of plaque vulnerability and there are
clear evidences that acute symptomatic plaques are always
carotid atherosclerotic plaques, embolization representing complicated, with low echogenicity and with relevant sur-
the main pathophysiological explanation. For this reason, face alterations. However, acute symptomatic plaques in
the identication of vulnerable lesions represents the fun- the very early phase have peculiar characteristics that are
damental step to select patients at risk of cerebrovascular possible to detect with careful US investigations. Their inci-
ischemic events from carotid disease where the surgical pro- dence is often underestimated while an accurate evaluation
cedure is indicated. This is a particularly relevant hot topic may be helpful to plan the most appropriate strategy to
in literature since optimal management of asymptomatic prevent further cerebrovascular events. Acute symptomatic
carotid stenosis still remains controversial [5], while the lesions have specic morphological aspects, and plaque rup-
benecial effect of CEA is recognized worldwide in symp- ture is a true adverse extremely unstable and common
tomatic patients for hemodynamic stenosis. However, the event in our experience in early phase. Data collected from
timing of surgery in acute cerebrovascular events is still recent studies indirectly conrm this condition: in the very
controversial. At present, early CEA is indeed the most acute stroke phase or in patients with transient ischemic
appropriate strategy to prevent further carotid cerebrovas- attacks, the risk of recurrency is signicantly higher and
cular events. CEA signicantly reduces the absolute risk of ipsilateral
Moreover, in particular, the aim of this short report is to ischemic stroke [9,10]. As recently indicated by Wardlow
focus on the utility of evaluating acute symptomatic lesions et al. [11], increasing delays to endarterectomy prevented
in the early phase, due to the possible detection of pecu- fewer strokes. In our experience, early ultrasonography
liar morphological aspects: plaque rupture is an unstable, performed with high resolution B-Mode imaging in real-time,
very common event, detected in our experience in all cases quickly revealed in all these symptomatic plaques harm-
admitted to the emergency area few hours from onset of ful characteristics, different from surface irregularities and
symptomatology. chronic ulcerations, or low echogenicity or low GSM.
The behavior of acute symptomatic plaques in the early Early admission to emergency-specic areas represents
phase is often underestimated, while an early and accu- the early care in hospitalized centers and the 24 h availabil-
rate evaluation may be helpful to plan the most appropriate ity of diagnostic facilities and operating rooms and vascular
strategy to prevent further cerebrovascular events. Further teams is a fundamental step to get a signicant improvement
efforts have to be performed to make a greater awareness of acute stroke patients prognosis. In conclusion, ultrasound
in patients so that they arrive in specialized areas as soon vascular imaging is a key component of the evaluation of
as possible: this is a crucial node. The onset of neurolog- early ischemic carotid diseases. Acute symptomatic plaques
ical symptomatology must be considered as an emergency are a well-dened entity that require early and accurate
condition. real-time evaluation, mandatory to thoroughly assess their
Advances of arterial imaging, through conventional radi- unstable behavior, rare, but highly risk condition. US imag-
ological imaging (CT and MR Angiography) [6,7] as well as ing, with high-resolution probes, harmonic imaging and
with ultrasonography [8], converge to achieve more detailed spatial compound, has the unique capability to assess these
information regarding the identication of these plaques. particular features in real-time, where immediate surgery
Summarizing, peculiar plaque characteristics such as severe may reduce further stroke risk.
Early ultrasound imaging of carotid arteries in the acute ischemic cerebrovascular patients 111

Conclusions [3] Giannoni MF, Vicenzini E, Citone M, Ricciardi MC, Irace L, Lau-
rito A, et al. Contrast carotid ultrasound for the detection of
unstable plaques with neoangiogenesis: a pilot study. Eur J Vasc
Timing of carotid endarterectomy has always been debated
Endovasc Surg 2009;37:7227.
in stroke patients clinical management, depending on sev- [4] Rigby H, Gubitz G, Phillips S. A systematic review of caregiver
eral factors, i.e. blood-brain-barrier breaking, neurological burden following stroke. Int J Stroke 2009;4:2859.
severity, entity of cerebral damage. All imaging techniques [5] Markus HS, King A, Shipley M, Topakian R, Cullinane M, Reihill
contribute to the identication of plaque morphology unsta- S, et al. Asymptomatic embolisation for prediction of stroke in
ble features, but early US has a crucial leading role in the Asymptomatic Carotid Emboli Study (ACES): a prospective
detecting plaque rupture and dynamic changes in real-time, observational study. Lancet Neurol 2010;9:66371.
allowing the identication of those lesions at particularly [6] Sadat U, Weerakkody RA, Bowden DJ, Young VE, Graves MJ,
high risk of further embolic events for their fragile charac- Li ZY, et al. Utility of high resolution MR imaging to assess
carotid plaque morphology: a comparison of acute symp-
teristics and that may benet from CEA performed early.
tomatic, recently symptomatic and asymptomatic patients
Acute symptomatic plaques require early and accurate
with carotid artery disease. Atherosclerosis 2009;207:4349.
real-time evaluation, mandatory to thoroughly assess their [7] Wintermark M, Arora S, Tong E, Vittinghoff E, Lau BC, Chien JD,
unstable behavior and successfully treat them. et al. Carotid plaque computed tomography imaging in stroke
and non-stroke patients. Ann Neurol 2008;64:14957.
Appendix A. Supplementary data [8] Vicenzini E, Giannoni MF, Ricciardi MC, Toscano M, Sirimarco
G, Di Piero V, et al. Non-invasive imaging of carotid arteries
in stroke: the emerging value of real-time, high resolution
Supplementary data associated with this arti- ultrasound in carotid occlusion due to cardiac embolism. J
cle can be found, in the online version, at Ultrasound Med 2010;29:163541.
doi:10.1016/j.permed.2012.02.045. [9] Coull AJ, Lovett JK, Rothwell PM, on behalf of the Oxford
Vascular Study. Population based study of early risk of stroke
after transient ischaemic attack or minor stroke: implica-
References tions for public education and organisation of services. BMJ
[1] Peeters W, Hellings WE, de Kleijn DP, de Vries JP, Moll FL, Vink [10] Eliasziw M, Kennedy J, Hill MD, Buchan AM, Barnett HJ,
A, et al. Carotid atherosclerotic plaques stabilize after stroke: North American Symptomatic Carotid Endarterectomy Trial
insights into the natural process of atherosclerotic plaque sta- Group. Early risk of stroke after a transient ischemic attack
bilization. Arterioscler Thromb Vasc Biol 2009;29:12833. in patients with internal carotid artery disease. Can Med Assoc
[2] Vicenzini E, Giannoni MF, Puccinelli F, Ricciardi MC, Altieri M, J 2004;170(March):11059.
Di Piero V, et al. Detection of carotid adventitial vasa vasorum [11] Wardlaw JM, Stevenson MD, Chappell F, Rothwell PM, Gillard
and plaque vascularization with ultrasound cadence contrast J, Young G, et al. Carotid artery imaging for secondary stroke
pulse sequencing technique and echocontrast agent. Stroke prevention: both imaging modality and rapid access to imaging
2007;38:28413. are important. Stroke 2009;40:35117.