個案報告 Vessel Wall Imaging to Differentiate Stroke Etiologies: Two Cases Report

Vessel Wall Imaging to Differentiate Stroke Etiologies:

Two Cases Report
Tsung-Ping Jeng1, Chih-Hao Chen2, Yu-Cheng Huang3, Sung-Chun Tang2

Departments of 1Medical Education, 2Neurology, 3Medical Imaging, National Taiwan University Hospital,
Taipei, Taiwan

ABSTRACT
Intracranial large artery disease (ILAD) has been a major contributing factor of ischemic strokes worldwide,
particularly in Asian populations. ILAD comprises of atherosclerotic and non-atherosclerotic origins,
which may require different treatment strategies. Non-atherosclerotic origins of ILAD, such as arterial
dissection, vasculitis, or Moyamoya disease, are often overlooked and underdiagnosed. In recent years, the
development of vessel wall imaging, such as high-resolution magnetic resonance image (MRI), enables
clinicians to depict and differentiate the underlying etiology of ILAD. Herein, we reported two cases
who had acute ischemic stroke due to middle cerebral artery stenosis, in which intracranial dissection and
atherosclerosis were diagnosed by vessel wall MRI respectively.

Keywords: high resolution MRI, intracranial dissection, intracranial large artery disease, vessel wall
imaging.

Introduction of conventional magnetic resonance imaging

Intracranial large artery disease(ILAD)
represents a major contributing factor of ischemic
strokes worldwide, 1, 2 particularly in Asian
3
populations. Of various etiologies, atherosclerotic
origin of ILAD, or intracranial atherosclerosis
(ICAS) plays a major role. On the other hand,
non-atherosclerotic origin of ILAD includes
but not limited to the following: intracranial
artery dissection, Moyamoya disease, vascular
inflammatory diseases, cerebral vasospasm,
and other immunological disorders. Despite
comprehensive medical survey and common use
(MRI), these non-atherosclerotic ILAD are often
overlooked and underdiagnosed, or may be
misclassified as having ICAS.4 A precise diagnosis
of vascular etiology can guide clinicians toward
appropriate treatment strategy in preventing
recurrent stroke. In recent years, high-resolution
MRI of cerebral vessel wall imaging has been
increasingly popular and provides an accurate
diagnosis of intracranial arterial lesions.5-7 In this
article, we reported two cases who had ischemic
strokes due to middle cerebral artery(MCA)
stenosis, and high resolution vessel wall MRI was
used to differentiate the vascular etiologies.

Corresponding author: Dr. Chih-Hao Chen, Department of Neurology, National Taiwan University Hospital, No. 7, Chung-
Shan South Road, Taipei 100, Taiwan, R.O.C.
E-mail: antonyneuro@gmail.com
DOI: 10.6318/FJS.202006_2(2).0007

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 Vessel Wall Imaging to Differentiate Stroke Etiologies: Two Cases Report

Case Report MRI for vessel wall imaging was performed

Case 1
A 41-year-old male patient without known
major systemic disease suffered from acute onset
of left limb weakness before night sleep, and the
symptom persisted after waking up in the next
morning. He also noted difficulty in swallowing,
asymmetric facial expression and unsteady gait.
He denied recent history of neck or head trauma.
He came to the emergency department, and the
initial National Institute of Health Stroke Scale
(NIHSS) score was 3. Brain computed tomography
(CT) did not show intracranial hemorrhage. Brain
MRI showed acute infarction in the posterior
limb of the right internal capsule, and magnetic
resonance angiography (MRA) showed right
MCA M1 segmental stenosis. Dual antiplatelet
therapy including Aspirin and Clopidogrel was
administered for mild symptoms of ischemic stroke
8
within 24 hours. His neurological status became
stable. A series of young stroke work-up were
performed but were unremarkable. High resolution
thereafter, and it showed a long segment stenosis
with intramural hematoma, and an abnormally
strong enhancement at the antero-superior aspect
of the right MCA wall (Figure 1). The picture was
highly suggestive of intracranial arterial dissection.
Then, dual antiplatelet therapy was shifted to
Aspirin alone. Subsequently, he had only minimal
left hemiparesis with a modified Rankin scale of 1
at hospital discharge.
Case 2
A 60-year-old male patient had no known
systemic disease, though he had smoked cigarette 1
pack per day for 40 years. He suffered acute onset
of left upper limb clumsiness, but he did not pay
attention to it initially. One week later, transient
inability to move his left leg upon standing
up ensued. There was no diplopia, drooling,
dysarthria, dysphagia or focal numbness. He then
visited emergency department, and initial NIHSS
score was 1. Non-contrast brain CT showed
hypodense lesions in the right frontoparietal
subcortical region without intracranial hemorrhage.

Fig. 1. Vessel wall imaging of intracranial dissection. (A) Longitudinal T1-weighted image (T1WI) showed
long segment luminal narrowing with smooth thickening in the anterior wall of right MCA (white
arrowheads), as opposed to normal appearing posterior wall (black arrowheads). (B) Multiplanar
reconstructed (MPR) T1WI aligned to the cross-sectional plane of affected vessel segment showed
eccentric wall thickening with high signal intensity at anterior wall of affected segment (white
arrowhead), indicating an intramural hematoma. (C) After intravenous contrast injection, overlay
image of enhanced portion showed strong enhancement at the dissected anterior wall (white arrow).

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 Vessel Wall Imaging to Differentiate Stroke Etiologies: Two Cases Report

Brain MRI revealed recent infarction at the right
fronto-parietal subcortical area and caudate
nucleus, and MRA showed right MCA M1
stenosis. For this patient, high resolution vessel
wall imaging of brain MRI revealed a segmental
stenosis in the right MCA M1 segment, presenting
as eccentric wall thickening with a contrast
enhancing plaque (Figure 2). ICAS related ILAD
was highly suspected. Atherosclerotic workup
showed serum total cholesterol 180 mg/dL, low
density lipoprotein cholesterol 107 mg/dL, fasting
glucose 110 mg/dL, and HbA1c 5.9%. Transcranial
color-coded ultrasonography showed increased
peak systolic velocity of 243 cm/s in the right
MCA. Dual antiplatelet therapy with Aspirin and
Clopidogrel was administered for intracranial
atherosclerotic disease, and smoking cessation
program was also initiated. His symptoms
improved, and no more transient ischemic attack
occurred as a result.
MRI protocol
High resolution vessel wall MRI images
are acquired on a 1.5 Tesla MRI scanner (Aera,
Siemens Healthcare, Erlangen, Germany) with 3D
T1-weighted SPACE (Sampling Perfection with
Application optimized Contrasts using different flip
angle Evolution) sequence. Scanning parameters
were: TR=900 ms, TE=22 ms, flip angle=120
degree, resolution: 0.4*0.4*0.8 mm.
Discussion
In this case report, both patients had
unambiguous MCA stenosis detected by
conventional MRA. Clinicians may incline to
make a diagnosis of ICAS when facing ILAD
because of its relatively high prevalence in Asian
populations, especially when the patients had
relevant vascular risk factors. However, making
such diagnosis based on medical speculation may
further lead to unnecessary and even harmful
interventions, such as prolonged dual antiplatelet
therapy or intracranial stenting.9 In the first case,
vessel wall imaging by high resolution MRI
unveiled an underlying MCA dissection, which
prompted the clinicians to stop dual antiplatelet
therapy because of its relatively benign course, and

Fig. 2. Vessel wall imaging of intracranial atherosclerosis. (A) Longitudinal T1-weighted image (T1WI)
after intravenous contrast injection showed short segment wall thickening in the anterior wall of
right MCA (white arrowheads). (B) Multiplanar reconstructed (MPR) T1WI aligned to the cross-
sectional plane of affected vessel segment showed eccentric wall thickening at anterior wall of
affected segment (white arrowhead) with isointense signal intensity to brain parenchyma. (C)
After intravenous contrast injection, strong enhancement at the affected anterior wall (white arrow)
indicated an active atherosclerotic lesion, likely to be the culprit lesion resulting in this stroke event.

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 Vessel Wall Imaging to Differentiate Stroke Etiologies: Two Cases Report
to avoid undesirable bleeding.10
Isolated MCA dissection is a rare yet
important cause of non-atherosclerotic etiology
of ILAD. The incidence of intracranial artery
dissection remains largely unknown but is believed
to be lower than that of cervical artery dissection,
11
about 2.6-3.0 per 100,000. It is reported more
commonly in Asians than Caucasian population,
which might be related to the anatomical and
genetic differences in vessel walls among
different ethnicities.4 Dissection in the anterior
circulation, such as MCA, usually presents with
luminal stenosis or occlusion and often leads to
ischemia, whereas vessel dissection in the posterior
circulation more commonly leads to formation of
dissecting aneurysms and subsequent subarachnoid
hemorrhage. 12 The reported cases of MCA
dissection were characterized by young age (<60
years old), male predominance, and no obvious
trauma history. Headache occurred in less than
half of the patients, and vascular risk factors were
12
also uncommonly presented. MCA dissection can
occur as an extension of cervical internal carotid
13
artery dissection, but can also arise in isolation.
Isolated MCA dissection usually takes place in
the M1 segment, which might be related to the
proximity between MCA and the bony sphenoid
13
ridge where friction related injury often occurs.
In our first patient case, isolated MCA segmental
stenosis in a young patient without attributable
vascular risk factors leads to the suspicion of MCA
dissection, and high resolution MRI was then
arranged.
Traditionally, gold standard for diagnosis of
MCA dissection relied on the digital subtraction
angiography (DSA). Pathognomonic luminal
findings of arterial dissection such as intimal
flap, double lumen appearance, or aneurysmal
formation, however, are seldom observed in the
intracranial dissection even by conventional
DSA.4 High resolution MRI can be advantageous
in delineating subtle changes in the small-caliber
intracranial vessel wall. Typical features of
intracranial dissection detected by high resolution
MRI include eccentric arterial wall thickening,
intimal flap (curvilinear T2 hyperintensity
separating true and false lumen), and intramural
hematoma (blood signal). 6 Of note, the signal
characteristics of intramural hematoma also
evolve over time such that hyperintensity in T1-
weighted image (representing methemoglobin)
usually takes place after 1 week.14 T2*-weighted
or susceptibility-weighted MRI can be useful in
detecting earlier change of blood component within
the intramural hematoma.15 Contrast enhancement
along the luminal and peripheral margins of the
artery wall can also be observed.6 As shown in one
single center case series, applying high resolution
MRI could identify about two thirds of intracranial
dissection that were previously misclassified as
having ICAS.16
The prognosis of isolated MCA dissection is
yet to be established but is usually believed to have
favorable outcome. Spontaneous recanalization
can be expected, and the risk of recurrent stroke
or progressive vascular stenosis is usually lower
than ICAS or Moyamoya disease. 4 Optimal
antithrombotic strategy for MCA dissection is
also unknown. However, in relatively young
patients without traditional vascular risk factors,
differentiating intracranial artery dissection from
ICAS by high resolution vessel wall imaging
can modify the treatment strategy, such that
complications from unnecessary long-term high-
intensity antiplatelets or statins use can be avoided.
On the other hand, ICAS is an important cause
of ischemic stroke and occurs disproportionately
higher in Asians than Caucasians. Advanced age,
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 Vessel Wall Imaging to Differentiate Stroke Etiologies: Two Cases Report
hypertension, diabetes mellitus, or metabolic
syndrome are all independent risk factors for
2
developing ICAS. Pathologically, ICAS related
atherosclerotic plaque is composed of lipids,
thrombotic substances such as platelet and fibrins,
cellular and extracellular matrix, and inflammatory
2
cells. In high resolution MRI, intracranial culprit
plaque typically causes an eccentric arterial wall
thickening. The components of plaque include
an enhancing layer (hyperintensity on T2, with
contrast enhancement) of fibrous cap adjacent to
the lumen, a non-enhancing and often hypointense
T2 layer of lipid core, with sometimes a peripheral
thin rim enhancement representing vasa vasorum,
which gives rise to a layered appearance. 6 Not
every intracranial plaque has such appearance, and
it may only cause an eccentric homogeneously
6
enhancing lump in the arterial wall. Enhancement
of intracranial plaque can be viewed as a marker
of inflammation and neovascularization, and has
been shown to be associated with ipsilateral recent
infarction.5, 17 Intraplaque hemorrhage, although
not as prevalent as in the extracranial carotid
18
plaque, can also reflect the plaque activity.
Using high resolution vessel wall MRI,
ILAD with eccentric wall thickening and contrast
enhancement can be seen in both intracranial
dissection and ICAS. However, certain imaging
features can still distinguish them (Table 1). For
example, presence of intramural hematoma and
Table 1. Imaging features in differentiating etiologies of intracranial large artery disease
Intracranial dissection
Predominant location Distal ICA, MCA, VA
Vessel stenosis Always
Vessel wall thickening Eccentric
Contrast enhancement Usually strong
Specific features Intramural hematoma, intimal flap
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intimal flap strongly suggests arterial dissection
as the cause, whereas layered plaque appearance
and intraplaque hemorrhage, if detected, may
hint toward ICAS as the underlying etiology. 7
Nevertheless, the culprit lesions are sometimes
difficult to clarify even by the help of vessel
wall imaging. Furthermore, certain pitfalls when
applying high resolution MRI still exist which
require optimal imaging technique and experienced
interpretation.
In conclusion, we presented two similar
cases of mild ischemic stroke with apparent MCA
stenosis. Further in-depth investigation using
vessel wall imaging disclosed different underlying
etiologies, one being atherosclerotic origin while
the other as non-atherosclerotic arterial dissection.
Continued efforts are needed to refine the
approach to ILAD diagnosis and to standardize the
application of intracranial vessel wall imaging.
Acknowledgements
We thanked Dr. Michael Yang for his great
help on the English editing.
Conflict of interest
None reported.
Intracranial atherosclerosis
Whole Willi’s circle
Not necessary
Eccentric
Variable
Layered plaque, intraplaque hemorrhage
 Vessel Wall Imaging to Differentiate Stroke Etiologies: Two Cases Report
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血管壁影像區別中風病因：二病例報告

鄭宗斌 1、陳志昊 2、黃裕城 3、湯頌君 2

台大醫院 1教學部、 2神經部、 3影像醫學部

摘　要
顱內大血管病變是缺血性中風重要原因，特別在亞洲族群比例偏高，顱內大血管病變包括動脈硬化
與非動脈硬化病因，非動脈硬化的顱內大血管病變主要包含動脈剝離、毛毛樣病變等，不同的病因
需要不同的臨床處置。近年來由於高解析度核磁共振影像的發展，顱內血管壁影像已經開始被用來
做為更精確的檢查。我們報告二位個案，初步皆診斷為中大腦動脈狹窄導致的急性缺血性中風，後
續藉由顱內血管壁影像檢查，確定一位為中大腦動脈剝離，另一位則是中大腦動脈粥狀硬化。高解
析度核磁共振的顱內血管壁影像可以做為更精準的顱內大血管病變的病因診斷。

關鍵詞：顱內大血管病變、顱內動脈剝離、高解析度核磁共振影像、血管壁影像

通訊作者：陳志昊醫師　台大醫院神經部
E-mail: antonyneuro@gmail.com

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