Abstracts
Objective
The potential of computed tomography angiography (CTA) was assessed for early determination of stroke subtypes in a Brazilian cohort of patients with stroke.
Method
From July 2011 to July 2013, we selected patients with suspected hyperacute stroke (< 6 hours). Intracranial and cervical arteries were scrutinized on CTA and their imaging features were correlated with concurrent subtype of stroke.
Results
Stroke was documented in 50/106 selected patients (47.2%) based on both clinical grounds and imaging follow-up (stroke group), with statistically significant arterial stenosis and vulnerable plaques on CTA. Intracranial large artery disease was demonstrated in 34% of patients in the stroke group. Partial territorial infarct prevailed (86%) while artery-to-artery embolization was the most common stroke mechanism (52%).
Conclusion
Multidetector CTA was useful for the etiologic work-up of hyperacute ischemic stroke and facilitated the knowledge about the topographic pattern of brain infarct in accordance with its causative mechanism.
tomography; MDCT; stroke; cerebral infarction
Objetivo
Avaliar o potencial da angiotomografia computadorizada multidetectores (ATCM) na determinação etiológica precoce do acidente vascular encefálico (AVE) e correlacionar o mecanismo causal com o padrão de infarto.
Método
De Julho de 2011 a Julho de 2013, foram selecionados os pacientes com suspeita clínica de AVE hiperagudo. Os achados da ATCM dos vasos intracranianos e cervicais foram correlacionados com a etiologia final do evento.
Resultados
AVE foi confirmado em 50/106 pacientes (47,2%). Estes apresentaram alterações angiográficas estatisticamente mais relevantes. Aterosclerose dos grandes vasos intracranianos esteve presente em 34% destes pacientes. O padrão radiológico topográfico de infarto mais comum foi o infarto territorial parcial (86%). A embolização arterio-arterial foi o mecanismo mais prevalente (52%).
Conclusão
A utilização da ATCM traz benefícios na detecção etiológica precoce dos pacientes com suspeita de AVE hiperagudo, além de possibilitar o entendimento do padrão radiológico topográfico de acordo com o mecanismo causal do evento isquêmico.
tomografia; ATCM; acidente vascular encefálico; infarto cerebral
Accurate classification of ischemic stroke based on etiology is essential for research
because stroke outcome, recurrent stroke rate, and strategies for secondary stroke
prevention differ according to stroke subtype11 Rothwell PM, Eliasziw M, Gutnikov SA, Fox AJ, Taylor DW, Mayberg MR
et al. Analysis of pooled data from the randomised controlled trials of
endarterectomy for symptomatic carotid stenosis. Lancet. 2003;361(9352):107-16.
http://dx.doi.org/10.1016/S0140-6736(03)12228-3
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,22 Kolominsky-Rabas PL, Weber M, Gefeller O, Neundoerfer B, Heuschmann
PU. Epidemiology of ischemic stroke subtypes according to TOAST criteria:
incidence, recurrence, and long-term survival in ischemic stroke subtypes: a
population-based study. Stroke. 2001;32(12):2735-40.
http://dx.doi.org/10.1161/hs1201.100209
https://doi.org/10.1161/hs1201.100209...
.
Furthermore, stroke subtype is used to describe patients’ characteristics in clinical
trials, group patients in epidemiological studies, phenotype patients in genetic
studies, and classify patients for therapeutic decision-making in daily practice22 Kolominsky-Rabas PL, Weber M, Gefeller O, Neundoerfer B, Heuschmann
PU. Epidemiology of ischemic stroke subtypes according to TOAST criteria:
incidence, recurrence, and long-term survival in ischemic stroke subtypes: a
population-based study. Stroke. 2001;32(12):2735-40.
http://dx.doi.org/10.1161/hs1201.100209
https://doi.org/10.1161/hs1201.100209...
,33 Amarenco P, Bogousslavsky J, Caplan LR, Donnan GA, Hennerici MG.
Classification of stroke subtypes. Cerebrovasc Dis. 2009;27(5):493-501.
http://dx.doi.org/10.1159/000210432
https://doi.org/10.1159/000210432...
,44 Bamford J, Sandercock P, Dennis M, Burn J, Warlow C. Classification
and natural history of clinically identifiable subtypes of cerebral infarction.
Lancet. 1991;337(8756):1521-6.
http://dx.doi.org/10.1016/0140-6736(91)93206-O
https://doi.org/10.1016/0140-6736(91)932...
. Topographic radiologic patterns of brain infarctions might
predict prognosis and correlate well with the underlying pathophysiology and imaging
findings55 Tei H, Uchiyama S, Ohara K, Kobayashi M, Uchiyama Y, Fukuzawa M.
Deteriorating ischemic stroke in 4 clinical categories classified by the
Oxfordshire Community Stroke Project. Stroke. 2000;31(9):2049-54.
http://dx.doi.org/10.1161/01.STR.31.9.2049
https://doi.org/10.1161/01.STR.31.9.2049...
.
Early determination of the etiologic factors of ischemic stroke is essential for
secondary prevention because the risk of recurrence is highly dependent on the
underlying cause66 Lovett JK, Coull AJ, Rothwell PM. Early risk of recurrence by
subtype of ischemic stroke in population-based incidence studies. Neurology.
2004;62(4):569-73.
http://dx.doi.org/10.1212/01.WNL.0000110311.09970.83
https://doi.org/10.1212/01.WNL.000011031...
,77 Oliveira Filho J, Martins SC, Pontes Neto OM, Longo A, Evaristo EF,
Carvalho JJ et al. Guidelines for acute ischemic stroke treatment: part I. Arq
Neuropsiquiatr. 2012;70(8):621-9.
http://dx.doi.org/10.1590/S0004-282X2012000800012
https://doi.org/10.1590/S0004-282X201200...
. Extra- or intra-cranial atheromas,
cardioembolic sources, and microvascular disease have been identified as the major
causes of ischemic stroke88 Ay H, Furie KL, Singhal A, Smith WS, Sorensen AG, Koroshetz WJ. An
evidence-based causative classification system for acute ischemic stroke. Ann
Neurol. 2005;58(5):688-97. http://dx.doi.org/10.1002/ana.20617
https://doi.org/10.1002/ana.20617...
,99 Yamamoto FI. Ischemic stroke in young adults: an overview of
etiological aspects. Arq Neuropsiquiatr. 2012;70(6):462-6.
http://dx.doi.org/10.1590/S0004-282X2012000600014
https://doi.org/10.1590/S0004-282X201200...
.
The proportions of patients with different ischemic stroke subtypes have been reported to
differ for each race-ethnic group1010 White H, Boden-Albala B, Wang C, Elkind MS, Rundek T, Wright CB et
al. Ischemic stroke subtype incidence among whites, blacks, and Hispanics: the
Northern Manhattan Study. Circulation. 2005;111(10):1327-31.
http://dx.doi.org/10.1161/01.CIR.0000157736.19739.D0
https://doi.org/10.1161/01.CIR.000015773...
,1111 Silva DA, Woon FP, Lee MP, Chen CP, Chang HM, Wong MC. South Asian
patients with ischemic stroke: intracranial large arteries are the predominant
site of disease. Stroke. 2007;38(9):2592-4.
http://dx.doi.org/10.1161/STROKEAHA.107.484584
https://doi.org/10.1161/STROKEAHA.107.48...
,1212 Lee PH, Oh SH, Bang OY, Joo SY, Joo IS, Huh K. Infarct patterns in
atherosclerotic middle cerebral artery versus internal carotid artery disease.
Neurology. 2004;62(8):1291-6.
http://dx.doi.org/10.1212/01.WNL.0000120761.57793.28
https://doi.org/10.1212/01.WNL.000012076...
. While Caucasians have an increased risk for cardioembolic
strokes1010 White H, Boden-Albala B, Wang C, Elkind MS, Rundek T, Wright CB et
al. Ischemic stroke subtype incidence among whites, blacks, and Hispanics: the
Northern Manhattan Study. Circulation. 2005;111(10):1327-31.
http://dx.doi.org/10.1161/01.CIR.0000157736.19739.D0
https://doi.org/10.1161/01.CIR.000015773...
, Asian patients with
ischemic stroke show increased incidence of intracranial large-artery disease
(ILAD)1111 Silva DA, Woon FP, Lee MP, Chen CP, Chang HM, Wong MC. South Asian
patients with ischemic stroke: intracranial large arteries are the predominant
site of disease. Stroke. 2007;38(9):2592-4.
http://dx.doi.org/10.1161/STROKEAHA.107.484584
https://doi.org/10.1161/STROKEAHA.107.48...
, and cervical arterial
disease is more often reported in western patients1212 Lee PH, Oh SH, Bang OY, Joo SY, Joo IS, Huh K. Infarct patterns in
atherosclerotic middle cerebral artery versus internal carotid artery disease.
Neurology. 2004;62(8):1291-6.
http://dx.doi.org/10.1212/01.WNL.0000120761.57793.28
https://doi.org/10.1212/01.WNL.000012076...
. In the Brazilian population, such differences remain
unclear.
Recent advances in computed tomography (CT) technology have improved the feasibility of
its use in clinical settings. Multidetector CT angiography (MDCTA) improves the
sensitivity and inter-rater reliability of detecting acute stroke1313 Scharf J, Brockmann MA, Daffertshofer M, Diepers M, Neumaier-Probst
E, Weiss C, et al. Improvement of sensitivity and interrater reliability to
detect acute stroke by dynamic perfusion computed tomography and computed
tomography angiography. J Comput Assist Tomogr. 2006;30(1):105-10.
http://dx.doi.org/10.1097/01.rct.0000187417.15321.ca
https://doi.org/10.1097/01.rct.000018741...
. In addition, it is an accurate and powerful
noninvasive tool for assessing carotid artery disease in the setting of hyperacute
ischemic stroke, including the detection of atherosclerosis involvement in extra- and
intra-cranial vessels. However, only a few studies have reported the use of MDCTA to
define stroke etiology in our population1414 Pacheco FT, Rocha AJ, Littig IA, Maia Junior AC, Gagliardi RJ.
Multiparametric multidetector computed tomography scanning on suspicion of
hyperacute ischemic stroke: validating a standardized protocol. Arq
Neuropsiquiatr. 2013;71(6):349-56.
http://dx.doi.org/10.1590/0004-282X20130037
https://doi.org/10.1590/0004-282X2013003...
. To the best of our knowledge, MDCTA has not yet been used to
study the etiology of stroke in a Latin American population.
In this study, we assessed the potential of the use of MDCTA for the early detection of the etiology of hyperacute ischemic stroke in the middle cerebral arteries (MCA) in a Brazilian cohort of patients and subsequently correlated the topography and causative mechanisms of infarcts.
METHOD
Patient selection
This study is part of a larger protocol in a single institution of the use of MDCTA techniques to evaluate hyperacute stroke, and the protocol has been reviewed and approved by the Institutional Review Board and the local ethics committee. From July 2011 to July 2013, adult patients (≥ 18 years old) who presented with hyperacute symptoms (< 6h) that were consistent with focal acute ischemia of the MCA and who had undergone CTA were considered eligible. The patient or their guardian signed the informed consent.
Patients with contraindications regarding intravenous iodine contrast administration were excluded from the study. In addition, we excluded patients who refused to participate in the study, patients with examinations with inadequate image quality, and patients who had posterior circulation strokes as their final diagnosis.
Protocol
All examinations were conducted with a previously reported institutional
protocol1414 Pacheco FT, Rocha AJ, Littig IA, Maia Junior AC, Gagliardi RJ.
Multiparametric multidetector computed tomography scanning on suspicion of
hyperacute ischemic stroke: validating a standardized protocol. Arq
Neuropsiquiatr. 2013;71(6):349-56.
http://dx.doi.org/10.1590/0004-282X20130037
https://doi.org/10.1590/0004-282X2013003...
with a minimum
dose of ionizing radiation and intravenous iodinated contrast in a Philips
Brilliance 64-slice CT scanner (Brilliance CT 64 Channel, Philips Medical,
Eindhoven, The Netherlands). The examinations included non-contrast computed
tomography and cervical and intracranial MDCTA, which required up to 5 min.
MDCTA was performed after intravenous administration of 50 mL of nonionic iodinated contrast (Ultravist®; 300 mg I/mL) at a rate of 5 mL/s using a dual-head power injector (Bayer HealthCare LLC, Whippany, NJ, USA) with an 18-G intravenous access, which was usually located in the cubital vein. The region of interest was placed in the aortic arch to determine the self-timer of the apparatus. When the attenuation in this region reached 160 HU, acquisition of the sections from the aortic arch to the vertex of the skull was initiated. Source images of CTA (CTA-SI) were postprocessed to obtain maximum intensity projections and three-dimensional views of the intracranial and extracranial arteries.
Analysis
All of the data were postprocessed with commercially available software on a workstation (Extended Brilliance Workspace v3.5.0.2250, Philips Medical Systems B.V., Best, The Netherlands). Two neuroradiologists who were experienced in vascular imaging and were blinded to the outcomes independently analyzed all of the CTA-SI from the emergency room examination and, subsequently, the maximum intensity projections and the three-dimensional reconstructions. All discrepancies were solved by consensus.
All patients were classified as having either normal or abnormal extracranial cervical carotid arteries. Vascular abnormalities that potentially correlated with concurrent stroke were discriminated based on their imaging features.
If a plaque was visible on CTA-SI, it was categorized based on the grade of
stenosis and type of plaque. The severity of stenosis was defined as the
remaining lumen at the site of stenosis as a percentage of the normal lumen
distal to the stenosis and categorized as < 50%, 50%-99%, and 100% (arterial
occlusion). The vessel diameters were measured on the plane that was
perpendicular to the vessel course. According to the TOAST criteria77 Oliveira Filho J, Martins SC, Pontes Neto OM, Longo A, Evaristo EF,
Carvalho JJ et al. Guidelines for acute ischemic stroke treatment: part I. Arq
Neuropsiquiatr. 2012;70(8):621-9.
http://dx.doi.org/10.1590/S0004-282X2012000800012
https://doi.org/10.1590/S0004-282X201200...
, we considered stenosis to be
relevant if the plaque resulted in a vessel diameter reduction of more than
50%.
The plaques’ morphologies were assessed subjectively by consensus, and their
densities were measured with the region of interest. The plaque composition was
analyzed according to the following previously proposed classification1515 Nandalur KR, Baskurt E, Hagspiel KD, Phillips CD, Kramer CM.
Calcified carotid atherosclerotic plaque is associated less with ischemic
symptoms than is noncalcified plaque on MDCT. Am J Roentgenol.
2005;184(1):295-8. http://dx.doi.org/10.2214/ajr.184.1.01840295
https://doi.org/10.2214/ajr.184.1.018402...
: (1) non-calcified plaques
(density, ≤ 50 HU), (2) calcified plaques (mean attenuation, > 130 HU), and
(3) mixed plaques (mean attenuation varying from 51 to 130 HU). For plaque
morphology analysis, its surface was considered regular or irregular. A stable
plaque was defined as a plaque that was calcified with a regular surface. If the
plaque was non-calcified or mixed and it had an irregular surface with or
without ulcerations, it was considered a vulnerable plaque.
The intracranial cerebrovascular system was scrutinized to be interpreted
according to current literature1111 Silva DA, Woon FP, Lee MP, Chen CP, Chang HM, Wong MC. South Asian
patients with ischemic stroke: intracranial large arteries are the predominant
site of disease. Stroke. 2007;38(9):2592-4.
http://dx.doi.org/10.1161/STROKEAHA.107.484584
https://doi.org/10.1161/STROKEAHA.107.48...
,1616 Wong KS, Huang YN, Gao S, Lam WW, Chan YL, Kay R. Intracranial
stenosis in Chinese patients with acute stroke. Neurology. 1998;50(3):812-3.
http://dx.doi.org/10.1212/WNL.50.3.812
https://doi.org/10.1212/WNL.50.3.812...
,1717 Lee DK, Kim JS, Kwon SU, Yoo SH, Kang DW. Lesion patterns and stroke
mechanism in atherosclerotic middle cerebral artery disease: early
diffusion-weighted imaging study. Stroke. 2005;36(12):2583-8.
http://dx.doi.org/10.1161/01.STR.0000189999.19948.14
https://doi.org/10.1161/01.STR.000018999...
. A diagnosis of atherothrombosis was assumed when
relevant cervical artery atherosclerosis was concomitant with a MCA thrombus.
However, a cardioembolic origin was determined when a cardiac source was
confirmed in the absence of relevant cervical artery disease. A diagnosis of
ILAD was adopted when partial or total atherosclerotic MCA obstruction was
documented in the absence of relevant cervical artery disease or cardioembolic
source. If was detected a non-relevant cervical artery disease combined with
partial or total atherosclerotic MCA obstruction was assumed that there was
concurrent ILAD and extracranial atherosclerosis. Follow-up images were analyzed
in order to confirm ischemic stroke. The topographic radiologic patterns of the
brain infarctions visible on non-contrast CT were defined with the OCSP
classification44 Bamford J, Sandercock P, Dennis M, Burn J, Warlow C. Classification
and natural history of clinically identifiable subtypes of cerebral infarction.
Lancet. 1991;337(8756):1521-6.
http://dx.doi.org/10.1016/0140-6736(91)93206-O
https://doi.org/10.1016/0140-6736(91)932...
, which
resulted in malignant, large, and limited infarcts for MCA territorial strokes.
Limited infarcts were those that covered only 1 of the 3 MCA territories (deep,
superficial anterior, or superficial posterior). Large infarcts were defined as
those covering at least 2 of these 3 MCA territories. Malignant infarction
referred to complete or almost complete MCA infarctions1818 Rovira A, GrivÉ E, Rovira A, Alvarez-Sabin J. Distribution
territories and causative mechanisms of ischemic stroke. Eur Radiol.
2005;15(3):416-26. http://dx.doi.org/10.1007/s00330-004-2633-5
https://doi.org/10.1007/s00330-004-2633-...
.
Finally, using the SSS-TOAST algorithm88 Ay H, Furie KL, Singhal A, Smith WS, Sorensen AG, Koroshetz WJ. An
evidence-based causative classification system for acute ischemic stroke. Ann
Neurol. 2005;58(5):688-97. http://dx.doi.org/10.1002/ana.20617
https://doi.org/10.1002/ana.20617...
, the patients were classified according to the results
of their individual examinations that included cervical Doppler ultrasonography,
cardiac echo, and electrocardiogram; this was termed the final
classification.
Statistical analysis
All of the information was entered into a database with Excel 2011 (Version 14.0.0; Microsoft Corporation, Redmond, WA, USA). We then entered all of the data into IBM SPSS Statistics software (Version 20.0 for Mac; IBM Corporation, Armonk, NY, USA). X2 tests were used to compare the variables between patients with and without brain infarctions and within the group of patients with brain infarctions. P-values less than 0.05 were considered statistically significant.
RESULTS
A total of 134 patients were recruited for this study. According to the previously reported criteria, 106 patients were selected for the retrospective analysis. They were divided according to their outcomes. An anterior circulation stroke was documented in 50/106 patients (47.2%) based on both clinical and imaging follow-up findings (stroke group), while 56/106 patients (52.8%) showed no evidence of brain ischemia (non-stroke group).
Unremarkable results on the cervical MDCTA were documented in 18 patients (18/50, 36.0%) patients in the stroke group. In the remaining patients, non-relevant stenosis was found in 17 patients (17/50, 34.0%) patients, while relevant stenosis in the cervical arteries was found in 15 patients (15/50, 30.0%) (Figure 1), including 5 patients (5/50, 10.0%) with stenosis diameters > 50%, 4 patients (4/50, 8.0%) with occlusive disease and the remaining 6 patients (6/50, 12.0%) with cervical arterial dissections.
A 56-year-old man presented within 60 minutes of a left hemiplegia. (A) Initial non-contrast CT with subtle hypoattenuating area in the MCA territory (arrowheads). Dotted line demonstrated a more extensive ischemic area according to the follow-up exam; (B) Follow-up imaging after 3 days demonstrated hypoattenuation in almost complete right MCA territory, which was compatible with brain ischemia as a result of artery-to-artery embolism; (C) Sagittal CTA MIP image demonstrated a heterogeneous plaque (arrow) determining severe luminal obstruction (90%); and (D) Axial imaging confirming the severe obstruction determined by heterogeneous plaque.
Conversely, relevant stenosis was only seen in 4 patients from the non-stroke group (4/56, 7.0%), while 20 patients (20/56, 36.0%) in this group had normal results on MDCTA. The remaining 32 (32/56, 57.0%) had only non-relevant stenosis (Χ2 test: p = 0.01; Table 1).
Although plaques may not cause relevant obstruction, they might be responsible for cerebral infarctions according to their characteristics. When patients with non-relevant stenosis were examined, 10 patients (10/17, 59.0%) in the stroke group were found to have vulnerable plaques. In contrast, 10 patients in the non-stroke group (10/32, 31.0%) were diagnosed with vulnerable plaques. (X2 test: p = 0.01; Table 1).
Of the 50 patients included in the stroke group, 7 (7/50, 14.0%) had normal intracranial and extracranial vessels. Imaging findings that were compatible with ILAD (Figure 2) were documented in 7 patients (7/50, 14.0%), while 12 (12/50, 24.0%) had only cervical carotid atherosclerosis and 10 (10/50, 20.0%) had concurrent ILAD and extracranial atherosclerosis. The remaining 14 patients (14/50, 28.0%) had atherothrombosis or cardioemboli with thrombi in the intracranial system. Of the 56 patients included in the non-stroke group, only 2 (2/56, 3.5%) had concurrent intra- and extra-cranial atherosclerosis, none had only intracranial disease, and 34 (34/56, 60.8%) had isolated extracranial disease (32 irrelevant stenosis and 2 relevant stenosis). Twenty patients (20/56, 35.7%) had unremarkable CTAs (X2 test: p = 0.01; Table 2).
An 80-year-old woman presented within 120 minutes of onset of left hemiplegia caused by ILAD. (A) Axial CTA MIP image demonstrated at least 50% stenosis in the right MCA. Dotted line demonstrated a more extensive ischemic area according to the follow-up exam; (B) Tridimensional (3D) view of the extracranial right carotid arteries only demonstrated parietal irregularities that corresponds a smalls calcified non-stenotic plaques; (C) Noncontrast CT demonstrated subtle effacement of the right insula (arrowheads). The dotted line demonstrated a more extensive ischemic area according to the follow-up exam; and (D) Imaging follow-up after 3 days demonstrated a large ischemic stroke in the MCA territory.
Based on the final classification using the SSS-TOAST algorithm, our patients were divided as: 25 (25/50, 50.0%) with large artery disease, 10 (10/50, 20.0%) with cardioemboli (Figure 3), 5 (5/50, 10.0%) with undetermined causes, 3 (3/50, 6.0%) with small-artery disease, 3 (3/50, 6.0%) with more than one evident mechanism, and 4 (4/50, 8.0%) with other causes (all of them cervical artery dissection) (Figure 4).
A 66-year-old man presented within 90 minutes of onset of right hemiplegia and aphasia. (A) Coronal CTA MIP image with unremarkable findings of the cervical carotid arteries; (B) Noncontrast CT demonstrates subtle effacement of the left insular cortex (arrowheads). Dotted line demonstrated a more extensive ischemic area according to the follow-up exam; and (C) Imaging follow-up after 2 days confirmed a large infarct in the MCA territory. A cardiac source of emboli was confirmed.
After reviewing the follow-up imaging, we classified the patients in the stroke group based on topographic radiologic patterns of brain infarction (OCSP classification). Forty-three (43/50, 86.0%) had territorial infarcts, of which 27 had limited, 7 had large, and 9 had malignant territorial infarcts; 3 (3/50, 6.0%) had centrum oval infarcts; 3 (3/50, 6.0%) had lacunar infarcts, and 1 (1/50, 2.0%) had a watershed infarct (Figure 5). When we analyzed the centrum oval infarcts, we found that all of them (3/3, 100.0%) were related to large artery atherosclerosis, while the lacunar infarcts (3/3, 100.0%) were due to small-artery occlusion. The only watershed infarct (1/1, 100.0%) was caused by cervical arterial dissection.
By correlating the OCSP and SSS-TOAST classifications we observed that cervical carotid atherosclerosis caused large or malignant brain infarctions in 6 patients (6/25, 24.0%), including 5 patients (5/6, 83.3%) with concurrent ILAD and extracranial disease. Large or malignant infarctions were also diagnosed in 6 patients with cardioemboli etiology (6/10, 60.0%) and in 2 patients with cervical arterial dissections (2/4, 50.0%).
DISCUSSION
Extracranial carotid atherosclerotic disease has been reported as the major risk
factor for stroke, and the main mechanism is related to artery-to-artery
embolization from either an atherosclerotic plaque or an acute occlusion of the
carotid artery with distal propagation of the thrombus1919 Saba L, Sanfilippo R, Pirisi R, Pascalis L, Montisci R, Mallarini G.
Multidetector-row CT angiography in the study of atherosclerotic carotid
arteries. Neuroradiology. 2007;49(8):623-37.
http://dx.doi.org/10.1007/s00234-007-0244-y
https://doi.org/10.1007/s00234-007-0244-...
. Accordingly, cervical carotid atherosclerotic
disease was demonstrated on CTA in the majority of our patients, and it was the main
risk factor for stroke with half of them presenting relevant stenosis or vulnerable
plaques on cervical arteries.
Luminal narrowing is the standard parameter used for reporting the severity of
carotid atherosclerosis2020 Magge R, Lau BC, Soares BP, Fischette S, Arora S, Tong E et al.
Clinical risk factors and CT imaging features of carotid atherosclerotic plaques
as predictors of new incident carotid ischemic stroke: a retrospective cohort
study. AJNR Am J Neuroradiol. 2013;34(2):402-9.
http://dx.doi.org/10.3174/ajnr.A3228
https://doi.org/10.3174/ajnr.A3228...
.
However, plaque morphology also plays an important role as it directly correlates
with the risk of embolism and occlusion, thus resulting in cerebral ischemia2121 Dawkins AA, Evans AL, Wattam J, Romanowski CA, Connolly DJ, Hodgson
TJ et al. Complications of cerebral angiography: a prospective analysis of 2,924
consecutive procedures. Neuroradiology. 2007;49(9):753-9.
http://dx.doi.org/10.1007/s00234-007-0252-y
https://doi.org/10.1007/s00234-007-0252-...
.
Several studies have highlighted that MDCTA findings closely correlate with those
from digital angiography for the degree of stenosis, which suggests that the
sensitivity of MDCTA in evaluating the degree of stenosis may be comparable to that
of angiography but with a lower level of risk2222 Ballotta E, Da Giau G, Renon L. Carotid plaque gross morphology and
clinical presentation: a prospective study of 457 carotid artery specimens. J
Surg Res. 2000;89(1):78-84.
http://dx.doi.org/10.1006/jsre.1999.5809
https://doi.org/10.1006/jsre.1999.5809...
,2323 Boussel L, Cakmak S, Wintermark M, Nighoghossian N, Loffroy R,
Coulon P et al. Ischemic stroke: etiologic work-up with multidetector CT of
heart and extra- and intracranial arteries. Radiology. 2011;258(1):206-12.
http://dx.doi.org/10.1148/radiol.10100804
https://doi.org/10.1148/radiol.10100804...
,2424 Lucas EM, Sánchez E, Gutiérrez A, Mandly AG, Ruiz E, Flórez AF et
al. CT protocol for acute stroke: tips and tricks for general radiologists.
Radiographics. 2008;28(6):1673-87.
http://dx.doi.org/10.1148/rg.286085502
https://doi.org/10.1148/rg.286085502...
,2525 Prokop M. Multislice CT angiography. Eur J Radiol. 2000;36(2):86-96.
http://dx.doi.org/10.1016/S0720-048X(00)00271-0
https://doi.org/10.1016/S0720-048X(00)00...
. The majority of the patients from our series
demonstrated some degree of cervical artery abnormalities that were detected on
MDCTA (64.0% in both groups). Our study confirmed that MDCTA was able to detect
relevant stenosis on cervical carotid arteries more commonly in patients with brain
infarcts (30.0% versus 7.0%) whose had the etiology of their
ischemic stroke defined in the same moment as the diagnosis of the brain
infarction.
Moreover, MDCTA detected vulnerable plaques, even in cases of non-relevant stenosis, in both groups. Although this finding was likely involved in the pathophysiology of the final infarct, further studies are necessary to confirm this. The relevance of the abnormal arteries on MDCTA in defining the stroke mechanism in the stroke group was well supported by our results. The relevance of cervical carotid abnormalities in patients from the non-stroke group (relevant stenosis or vulnerable plaques) remains uncertain as these findings could be related to either transient ischemic attacks or minor infarcts with absent brain lesions or abnormalities not detectable on brain CT.
In patients with non-relevant abnormalities, the percentages of plaques were the same
in both groups, but analyzing the characteristics of the plaques on cervical CTA
showed that the percentage of the vulnerable plaque type was higher in the stroke
group (59.0% versus 21.0%), which corroborated data aggregated by
Gupta et al. in a meta-analysis that suggested an association of these types of
plaques with an increased risk of stroke2626 Gupta A, Baradaran H, Schweitzer AD, Kamel H, Pandya A, Delgado D et
al. Carotid plaque MRI and stroke risk: a systematic review and meta-analysis.
Stroke. 2013;44(11):3071-7.
http://dx.doi.org/10.1161/STROKEAHA.113.002551
https://doi.org/10.1161/STROKEAHA.113.00...
. Considering these characteristics, our findings
corroborated that it is important to examine plaque morphology in addition to the
lumen obstruction1111 Silva DA, Woon FP, Lee MP, Chen CP, Chang HM, Wong MC. South Asian
patients with ischemic stroke: intracranial large arteries are the predominant
site of disease. Stroke. 2007;38(9):2592-4.
http://dx.doi.org/10.1161/STROKEAHA.107.484584
https://doi.org/10.1161/STROKEAHA.107.48...
.
Large artery atherosclerosis was the main stroke type in our group of patients, and
it involved 50.0% of the cases. Limited infarction was the most common imaging
finding. This finding demonstrates a slightly higher prevalence of carotid
atherosclerotic disease as a cause for stroke than those previously postulated22 Kolominsky-Rabas PL, Weber M, Gefeller O, Neundoerfer B, Heuschmann
PU. Epidemiology of ischemic stroke subtypes according to TOAST criteria:
incidence, recurrence, and long-term survival in ischemic stroke subtypes: a
population-based study. Stroke. 2001;32(12):2735-40.
http://dx.doi.org/10.1161/hs1201.100209
https://doi.org/10.1161/hs1201.100209...
,2020 Magge R, Lau BC, Soares BP, Fischette S, Arora S, Tong E et al.
Clinical risk factors and CT imaging features of carotid atherosclerotic plaques
as predictors of new incident carotid ischemic stroke: a retrospective cohort
study. AJNR Am J Neuroradiol. 2013;34(2):402-9.
http://dx.doi.org/10.3174/ajnr.A3228
https://doi.org/10.3174/ajnr.A3228...
,2727 Ois A, Cuadrado-Godia E, Rodríguez-Campello A, Giralt-Steinhauer E,
Jiménez-Conde J, Lopez-Cuiña M et al. Relevance of stroke subtype in vascular
risk prediction. Neurology. 2013;81(6):575-80.
http://dx.doi.org/10.1212/WNL.0b013e31829e6f37
https://doi.org/10.1212/WNL.0b013e31829e...
. A more precise elucidation of the role of vulnerable
plaques in non-relevant stenosis and their implications in the absence of concurrent
brain infarcts detectable on CT remains uncertain.
Atherosclerosis MCA and ICA disease have been associated with racial differences.
While MCA disease is often reported in Asians, ICA disease is frequently found in
western populations2828 Lee SJ, Cho SJ, Moon HS, Shon YM, Lee KH, Kim DI et al. Combined
extracranial and intracranial atherosclerosis in Korean patients. Arch Neurol.
2003;60(11):1561-4.
http://dx.doi.org/10.1001/archneur.60.11.1561
https://doi.org/10.1001/archneur.60.11.1...
. Man et
al.2929 Man BL, Fu YP, Chan YY, Lam W, Hui AC, Leung WH et al. Lesion
patterns and stroke mechanisms in concurrent atherosclerosis of intracranial and
extracranial vessels. Stroke. 2009;40(10):3211-5.
http://dx.doi.org/10.1161/STROKEAHA.109.557041
https://doi.org/10.1161/STROKEAHA.109.55...
found that 72% of a
Chinese cohort of patients had ILAD, which differed from the findings in our patient
group, in which 34% had ILAD; 14% had ILAD and 20.0% had ILAD along with cervical
arterial disease. Thus, similar to the results from other countries of the western
world, our Brazilian patients population more frequently had ICA disease as a
well-defined stroke subtype. Despite that, ILAD was largely documented in our series
of patients with hyperacute stroke that was isolated or in association with
extracranial atherosclerosis, which suggested a relationship between the severity of
atherosclerosis in Brazilian patients and the causative factor of clinical stroke.
In a majority of our cases, ILAD caused a limited infarct that was similar to
cervical atherosclerosis. Otherwise, patients who had these concomitant conditions
developed a large or malignant infarct more frequently, which conflicted with the
data reported by Man et al.2121 Dawkins AA, Evans AL, Wattam J, Romanowski CA, Connolly DJ, Hodgson
TJ et al. Complications of cerebral angiography: a prospective analysis of 2,924
consecutive procedures. Neuroradiology. 2007;49(9):753-9.
http://dx.doi.org/10.1007/s00234-007-0252-y
https://doi.org/10.1007/s00234-007-0252-...
.
Considering the OCSP classifications in our subgroup of patients, territorial infarcts prevailed (86.0%). Of these, 32.0% were large or malignant infarcts, which exhibited a higher frequency of clinical deterioration, a minimum chance of better outcome, and a high mortality rate. In patients with large infarcts, the frequency of cardioembolic disease was clearly higher than in those with small brain lesions. Hypothetically, because cardioembolic thrombi tend to be larger, they might stop proximally in the intracranial circulation.
This study’s strengths include the use of a new CT technique that is safe and minimally invasive and that is able to evaluate stroke mechanisms and vascular etiology. This protocol is reproducible because MDCTA is widely available and often applicable in hyperacute settings in emergency rooms.
This study had several limitations, including a small sample size, experience based
on a single institution, restriction to MCA infarcts, and absence of clinical
information. The use of CT for follow-up imaging in our patients might limit the
detection of brain lesions, particularly transient ischemic attacks or minor
infarcts, and the extension of brain infarcts, which is useful for defining their
topography and subtypes. CT has been used in similar reports that have evaluated
intracranial and cervical stenosis in hyperacute brain infarcts1111 Silva DA, Woon FP, Lee MP, Chen CP, Chang HM, Wong MC. South Asian
patients with ischemic stroke: intracranial large arteries are the predominant
site of disease. Stroke. 2007;38(9):2592-4.
http://dx.doi.org/10.1161/STROKEAHA.107.484584
https://doi.org/10.1161/STROKEAHA.107.48...
,3030 Silva DA, Woon FP, Pin LM, Chen CP, Chang HM, Wong MC. Intracranial
large artery disease among OCSP subtypes in ethnic South Asian ischemic stroke
patients. J Neurol Sci. 2007;260(1-2):147-9.
http://dx.doi.org/10.1016/j.jns.2007.04.020
https://doi.org/10.1016/j.jns.2007.04.02...
. Although the use of diffusion-weighted imaging has
been advocated to be more accurate in detecting brain ischemia and exploring stroke
mechanisms, this technique is not included as part of the routine workup in patients
with hyperacute stroke1212 Lee PH, Oh SH, Bang OY, Joo SY, Joo IS, Huh K. Infarct patterns in
atherosclerotic middle cerebral artery versus internal carotid artery disease.
Neurology. 2004;62(8):1291-6.
http://dx.doi.org/10.1212/01.WNL.0000120761.57793.28
https://doi.org/10.1212/01.WNL.000012076...
,2929 Man BL, Fu YP, Chan YY, Lam W, Hui AC, Leung WH et al. Lesion
patterns and stroke mechanisms in concurrent atherosclerosis of intracranial and
extracranial vessels. Stroke. 2009;40(10):3211-5.
http://dx.doi.org/10.1161/STROKEAHA.109.557041
https://doi.org/10.1161/STROKEAHA.109.55...
,3131 Bang OY, Lee PH, Heo KG, Joo US, Yoon SR, Kim SY. Specific DWI
lesion patterns predict prognosis after acute ischaemic stroke within the MCA
territory. J Neurol Neurosurg Psychiatry. 2005;76(9):1222-8.
http://dx.doi.org/10.1136/jnnp.2004.059998
https://doi.org/10.1136/jnnp.2004.059998...
. Brain CT is preferred in our institutional protocol for
evaluating hyperacute brain ischemia in the anterior intracranial circulation.
Despite these limitations, this study provided unique data on the relationship between infarct patterns on brain imaging and the likely mechanisms of stroke in a cohort of Brazilian patients.
In conclusion, MDCTA is useful for the etiologic examination of patients with acute ischemic strokes in order to plan future clinical trials for the prevention and treatment of this disorder in Latin American patients. Our data confirmed that patients with suspected hyperacute brain infarcts in the MCA territory could benefit from having MDCTA added to the imaging protocol as a fast, minimally invasive, widely available, and reliable tool for the early determination of the main etiologic factors.
This study suggested that artery-to artery embolization was the most common stroke mechanism in patients with relevant cervical carotid stenosis. Conversely, the absence of cervical carotid abnormalities favored the cardioembolic mechanism with larger brain infarcts. ILAD seems to be a common etiology for stroke, and it correlated with the severity of atherosclerosis in this series of Brazilian patients.
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» https://doi.org/10.1161/STROKEAHA.109.557041 -
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» https://doi.org/10.1016/j.jns.2007.04.020 -
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» https://doi.org/10.1136/jnnp.2004.059998
Publication Dates
-
Publication in this collection
May 2015
History
-
Received
05 Sept 2014 -
Received
08 Jan 2015 -
Accepted
28 Jan 2015