J Neurosurg 121:631–636, 2014
©AANS, 2014

Emergent surgical embolectomy for middle cerebral artery
occlusion due to carotid plaque rupture followed by elective
carotid endarterectomy
Case report
Satoshi Kiyofuji, M.D., Tomohiro Inoue, M.D., Hirotaka Hasegawa, M.D.,
Akira Tamura, M.D., Ph.D., and Isamu Saito, M.D., Ph.D.
Department of Neurosurgery, Fuji Brain Institute and Hospital, Fujinomiya City, Shizuoka, Japan
Embolic intracranial large artery occlusion with severe neurological deficit is associated with an extremely poor
prognosis. The safest and most effective treatment strategy has not yet been determined when such emboli are associated with unstable proximal carotid plaque. The authors performed emergent surgical embolectomy for left middle
cerebral artery (MCA) occlusion, and the patient experienced marked neurological recovery without focal deficit
and regained premorbid activity. Postoperative investigation revealed “vulnerable plaque” of the left internal carotid
artery without apparent evidence of cardiac embolism, such as would be seen with atrial fibrillation. Specimens
from subsequent elective carotid endarterectomy (CEA) showed ruptured vulnerable plaque that was histologically
consistent as a source of the intracranial embolic specimen. Surgical embolectomy for MCA occlusion due to carotid
plaque rupture followed by CEA could be a safer and more effective alternative to endovascular treatment from the
standpoint of obviating the risk of secondary embolism that could otherwise occur as a result of the manipulation of
devices through an extremely unstable portion of plaque. Further, this strategy is associated with a high probability
of complete recanalization with direct removal of hard and large, though fragile, emboli.
(http://thejns.org/doi/abs/10.3171/2014.4.JNS132441)

Key Words
•
acute ischemic stroke
•
carotid endarterectomy
•
embolectomy
vascular disorders

A

lthough traditional direct surgical embolectomy

through a craniotomy for acute ischemic stroke
has been performed since the 1950s,9,18 intravenous administration of tissue plasminogen activator and
endovascular methods have become recognized as faster
and are now the gold-standard treatment for embolism.
Most recently, endovascular treatment for acute intracranial large artery occlusion has benefitted from the introduction of new devices, such as the MERCI retriever,

Abbreviations used in this paper: CAS = carotid artery stenting;
CEA = carotid endarterectomy; DSA = digital subtraction angiography; DWI = diffusion-weighted imaging; ECG = electrocardiogram;
ICA = internal carotid artery; MCA = middle cerebral artery; MRA
= MR angiography; NIHSS = National Institutes of Health Stroke
Scale; TIMI = Thrombolysis in Myocardial Infarction.

J Neurosurg / Volume 121 / September 2014

intracranial embolism •
•
internal carotid artery stenosis

•

the Penumbra system, and the Solitaire stent.2,12,13 Recent
endovascular embolectomy devices have been used to accomplish up to 80%–90% recanalization rates (Thrombolysis in Myocardial Infarction [TIMI] Grades 2–3), but
the complete recanalization rate (TIMI Grade 3) achieved
with such devices is not satisfactory, especially when the
clot burden is high.2,10,12,17 By contrast, a recent report of
surgical embolectomy demonstrated a high complete recanalization rate and an acceptable safety profile, especially when using MRI to select appropriate patients.5
Among cases of devastating acute intracranial large
artery occlusion, those arising from intracranial emboli
associated with carotid plaque rupture are rare. Given
the possible high embolic clot burden associated with
ruptured plaque and secondary engrafted thrombus, the
treatment strategy for this situation remains controversial.
631

S. Kiyofuji et al.
Furthermore, because of proximal, extremely unstable
plaque, it can be quite difficult to deploy the endovascular
device without generating additional emboli.
In the present report we describe a unique case of
emergent direct surgical embolectomy through a craniotomy for occlusion caused by ruptured carotid plaque,
followed by elective carotid endarterectomy (CEA) to
prevent further stroke associated with the extremely unstable plaque.

Case Report
History and Examination. A 78-year-old woman
with a history of hypertension suddenly collapsed at
home and was transported by ambulance to our hospital.
She was taking antihypertensive drugs only and had never been treated with any antiplatelet or anticoagulation
drugs. Upon arrival, she showed right hemiplegia, global
aphasia, and conjugate deviation of her eyes to the left.
Her National Institutes of Health Stroke Scale (NIHSS)
score was 17.
Initial CT showed abnormal high-density signal in
the bifurcation of the left middle cerebral artery (MCA),
suggestive of some calcified embolus, without any signs
of early ischemia (Fig. 1A and B). She was taken to the
MRI suite where MR angiography (MRA) demonstrated
an occluded M1 on the left, while diffusion-weighted imaging (DWI) showed only minimal ischemia with spotty

high-signal-intensity lesions in the left insular cortex,
frontal lobe, and temporal lobe (Fig. 1C–F). Since there
was a mismatch between the expected infarction area on
MRA and actual lesions on DWI, as well as a mismatch
between severe neurological symptoms and minimal lesions on DWI, emergent recanalization treatment was
indicated.8,16 Considering the potentially highly calcified
appearance of embolic material on CT that could be refractory to the pharmacological effect of intravenous tissue plasminogen activator, in addition to the fact that endovascular service is not available in emergent settings at
our institution, we decided, based on our experience with
high complete recanalization rates in such procedures, to
proceed with emergent surgical embolectomy.5 After a
thorough discussion with her family, we started the operation 1.5 hours after the patient’s arrival at our hospital.
First Operation. The procedure was conducted as
described in detail elsewhere.5 In short, through a left
frontotemporal craniotomy, the left MCA bifurcation was
exposed. A whitish thrombus was seen from outside the
MCA bifurcation (Fig. 2A). A transverse incision was
made in the bifurcation, and the apparently partially calcified, hard though fragile embolus was completely removed (Fig. 2B). The incision was sutured with 9-0 nylon (Fig. 2C). Complete recanalization (TIMI Grade 3)
was confirmed intraoperatively with an ultrasound Doppler flow meter and immediately postoperatively with an
MRA study (Fig. 3). The recanalization time was 42 min-

Fig. 1. Images obtained at patient’s arrival, before the embolectomy. Head CT (A) shows an abnormal high-density lesion
(arrow) in the left MCA. The Hounsfield unit count of the emboli (arrow) is 164.9, while those of the sphenoid ridge (bone) and
contralateral MCA are 403.2 and 26.4, respectively (B). The left MCA is occluded at M1 (C, arrow), and diffusion-weighted images
(D–F) demonstrate high-intensity lesions in the insula, frontal lobe, and temporal lobe.

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J Neurosurg / Volume 121 / September 2014

Surgical embolectomy followed by carotid endarterectomy

Fig. 2. Intraoperative views of the embolectomy. A white thrombus (A, arrow, near center of image) appeared in the MCA
bifurcation and was resected (B). Arteriotomy at the bifurcation was sutured after resection of the thrombus (C).

utes from the start of surgery, 2 hours 32 minutes since
the arrival of the patient, and approximately 3 hours 30
minutes since symptom onset.

First Postoperative Course. Postoperatively, the patient showed marked neurological recovery without additional lesions on DWI. She had full restoration of motor
function, resulting in an improvement in her NIHSS score
from 17 to 5 at 3 weeks postoperatively. Although preoperative and intraoperative electrocardiogram (ECG) did
not show atrial fibrillation, a chest radiograph at admission
revealed left ventricular hypertrophy. Therefore, we evaluated for possible cardiac embolic causes. Holter ECG and
chest ultrasonography by a cardiologist were essentially
negative, and thus there was no persuasive evidence of a
cardiogenic event. Meanwhile, neck MRI showed only
moderate carotid stenosis with a slightly high-intensity lesion in the left carotid plaque on magnetization-prepared
rapid acquisition of gradient echo (MPRAGE) imaging,
suggesting possible unstable plaque deposition (Fig. 4A–

D).20 We proceeded with digital subtraction angiography
(DSA), which demonstrated intermediate stenosis and an
irregularly surfaced left internal carotid artery (ICA) with
ulceration consistent with ruptured plaque (Fig. 4E). Given
these findings, we suspected that the left ICA plaque was
the cause of the M1 embolus. At that time, since the patient
had regained her premorbid level of activities of daily living, which included ambulating and eating as usual, and
after a thorough discussion with her and her family, we
decided to proceed with elective carotid endarterectomy
(CEA) to remove the embolic origin.
Second Operation. The CEA was performed 3 weeks
after the surgical embolectomy. Video 1 features actual
procedures of the surgical embolectomy and subsequent
CEA.

Video 1. Clip demonstrates actual procedures of the surgical
embolectomy and subsequent CEA. Copyright Satoshi Kiyofuji.
Published with permission. Click here to view with Media
Player. Click here to view with Quicktime.

The plaque of the carotid artery is shown in Fig. 5.
There were significantly calcified lesions in the plaque,
which resembled the embolus in her left MCA bifurcation. Pathological investigation showed similarities between the MCA embolus and the carotid plaque component and revealed that the two specimens were almost
identical pathologically.
Second Postoperative Course. Postoperative DWI
did not show any additional ischemic lesion, and MRA
demonstrated a smooth and widely patent left carotid
artery. Antiplatelet therapy was started postoperatively
instead of anticoagulation therapy, and rehabilitation
enabled the patient to live independently. At 6 months
postoperatively, her modified Rankin Scale score was 1
without focal neurological deficit.

Discussion

Fig. 3. Magnetic resonance angiogram obtained after the embolectomy. Full recovery of the blood flow of the left MCA was achieved.

J Neurosurg / Volume 121 / September 2014

Sudden and extremely severe clinical manifestations
in patients with ischemic stroke can suggest cardiac embolism associated with atrial fibrillation. About 30% of
strokes are associated with atrial fibrillation, and such
strokes tend to be devastating.3 Thus, in the featured patient, we initially assumed that the removed embolus was
of cardiac origin given the sudden onset of her symptoms,
severe neurological deficits, and concomitant cardiomeg633

S. Kiyofuji et al.

Fig. 4. Magnetic resonance angiograms (A–D) of the neck and DS angiogram (E) of the left ICA. Magnetic resonance angiogram of the neck shows the irregular surface of the left ICA (A, arrow), and an MPRAGE image shows high-intensity plaque (B,
arrow), which is isointense to low intensity on a T1-weighted image (C, arrow) and isointense to high intensity on a T2-weighted
image (D, arrow). Left ICA stenosis was seen on DSA (E, arrow).

aly. Therefore, anticoagulation therapy with heparin followed by warfarinization was started in response to presumed paroxysmal atrial fibrillation. However, a negative
postoperative cardiac evaluation directed our attention to
the cervical portion of the carotid artery as a possible em-

Fig. 5. Intraoperative view during the CEA. Calcified yellow plaque
was present in the internal lumen (arrow), part of which resembled the
thrombus that had been resected in the embolectomy (Fig. 2B). An ulcerative lesion was also visible (arrowhead).

634

bolic source, despite the fact that cervical MRA showed
only low-grade carotid stenosis. Finally, imaging of the
plaque using MRI in conjunction with conventional DSA
revealed left low-grade carotid stenosis with “vulnerable
plaque” as the cause of the embolus. It is quite rare to
find that the embolus removed in a surgical embolectomy
resembles the ruptured irregular surface and/or contents
of the carotid plaque in CEA. Both specimens were hard,
yellow, and highly calcified. The pathology report confirmed that the embolus was identical to the ICA plaque
in terms of histological features, that is, a highly calcified
lesion in the background of some cholesterol crystals. A
recent report demonstrated a high rate of recurrent microembolic events, even in low-grade carotid stenosis, once
a patient became symptomatic. Indeed, the contents of
the plaque were judged as unstable, according to MRI.20
Thus, we need to consider the possibility that even lowgrade carotid stenosis can cause large intracranial emboli, especially when emboli of cardiac origin are excluded.
Although there are some case reports on the endovascular removal of distal emboli associated with carotid
artery stenting (CAS), direct microsurgical embolectomy
of emboli originating from an ICA plaque rupture is
quite rare.1,15 Given a potential high clot burden of emboli released from ruptured carotid plaque and the hard
but fragile nature of the mixture of calcified plaque with
secondary engrafted fibrin clot, it might be difficult to
J Neurosurg / Volume 121 / September 2014

Surgical embolectomy followed by carotid endarterectomy
achieve appropriate recanalization by pharmacological
thrombolysis or endovascular methods. In fact, one study
demonstrated that emboli composed of platelet, atheroma,
and cellular debris are more resistant than erythrocyterich emboli to any revascularization treatment whether it
consists of a fibrinolytic agent, mechanical endovascular
embolectomy, or a combination of the two.11 The unusually high Hounsfield unit count and accompanying calcified
appearance of the emboli were quite unlikely to be those
of simple erythrocyte-rich emboli. By contrast, the high
complete recanalization rate and the acceptable safety
profile of surgical embolectomy through a craniotomy,
regardless of the embolic clot burden, have recently been
described.5,14 The safety of the access to an embolic lesion
should also be considered. In cases of intracranial major
artery embolism coinciding with extremely unstable carotid plaque and possible rupture, endovascular removal
of the emboli could involve high risk. If a catheter or
guidewire passes through the plaque portion, a thrombus
attached to the vulnerable plaque could migrate, causing further distal intracranial embolism. Carotid artery
stenting could be tried before removal of the intracranial
embolus, but CAS itself is associated with a high risk of
distal embolism, especially when the plaque is fragile
with ulceration or hemorrhage.4,7 Surgical embolectomy
through a craniotomy could be performed to avoid the
risk of irritating the vulnerable carotid plaque, while also
minimizing the risk of distal emboli during embolectomy,
since temporary clips are applied in distal arteries before
the removal of emboli.5 Furthermore, in the present case,
we preclamped the external carotid artery and common
carotid artery to prevent microemboli during the dissection phase of the CEA, which effectively prevented even
asymptomatic ischemia, as confirmed on postoperative
DWI.6,19 Thus, in cases of intracranial emboli associated
with the deposition of unstable carotid plaque, direct surgical embolectomy followed by CEA could have advantages over endovascular treatment from the standpoint of
preventing further ischemic events during intervention.
The issue of time to reperfusion should be addressed.
In theory, surgical embolectomy may take longer than
endovascular methods. This is because endovascular
methods can be used to achieve recanalization essentially
within the same procedure and immediately following
diagnostic DSA, whereas surgical embolectomy requires
transfer of the patient from the radiology suite to the operating room. To minimize time loss, we made an effort
to transport patients directly from the MRI suite to the
operating room. Standard frontotemporal craniotomy
with minimal hemostasis required about 20 minutes, and
in the present case we were able to accomplish recanalization in 42 minutes since the start of surgery and in 2
hours 32 minutes since the patient arrived at our hospital, which, we believe, would compare favorably with the
time to recanalization associated with the endovascular
method.5
Disclosure
The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this
paper.

J Neurosurg / Volume 121 / September 2014

Author contributions to the study and manuscript preparation
include the following. Conception and design: Inoue. Acquisition
of data: Kiyofuji. Drafting the article: Kiyofuji. Critically revising
the article: all authors. Reviewed submitted version of manuscript:
all authors. Approved the final version of the manuscript on behalf
of all authors: Kiyofuji. Administrative/technical/material support:
Hasegawa, Tamura, Saito.
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Manuscript submitted November 3, 2013.
Accepted April 30, 2014.
Please include this information when citing this paper: published online June 6, 2014; DOI: 10.3171/2014.4.JNS132441.
Supplemental online information:
Video: http://mfile.akamai.com/21490/wmv/digitalwbc.download.
akamai.com/21492/wm.digitalsource-na-regional/jns13-2441_
video.asx (Media Player).
http://mfile.akamai.com/21488/mov/digitalwbc.download.akamai.
com/21492/qt.digitalsource-global/jns13-2441_video.mov
(Quicktime).
Address correspondence to: Satoshi Kiyofuji, M.D., Department
of Neurosurgery, Fuji Brain Institute and Hospital, 270-12 Sugita,
Fujinomiya City, Shizuoka 418-0021, Japan. email: kiyofuji-tky@
umin.ac.jp.

J Neurosurg / Volume 121 / September 2014