Case report

Reocclusion of the treated vessel due to endothelial
injury after mechanical thrombectomy in a patient
with acute ischaemic stroke
Masaoki Hidaka,1 Shinya Yamaguchi,2 Yuya Koyanagi,2 Shuji Arakawa1
1

Department of Cerebrovascular
Disease, Nippon Steel Yawata
Memorial Hospital, Kitakyushu,
Japan
2
Department of Neurosurgery,
Nippon Steel Yawata Memorial
Hospital, Kitakyushu, Japan
Correspondence to
Dr Masaoki Hidaka,
​MasaokiHidaka@​gmail.​com
Accepted 19 July 2019

Summary
A 92-year-old woman developed sudden consciousness
disturbance, global aphasia and right hemiparesis.
She had atrial fibrillation and cardioembolic stroke
was diagnosed. Tissue plasminogen activator was
administered, and endovascular treatment was
initiated. The left middle cerebral artery was occluded
and complete recanalisation was achieved after
direct aspiration first-pass technique. However, MRI
immediately after treatment showed reocclusion.
Endovascular treatment was repeated and complete
recanalisation was achieved. There was no evidence of
cerebral artery dissection, but angiography soon after the
second procedure revealed early reocclusion. Ozagrel,
an antiplatelet agent, was administered intravenously
and prevented reocclusion. Endothelial injury was
speculated to have occurred during the first mechanical
thrombectomy, leading to recurrent occlusion. Though
the patient continued to have right hemiparesis, she
recovered from her consciousness disturbance and
aphasia after re-treatment.

Background
A meta-analysis of randomised trials showed that
mechanical thrombectomy using specific devices for
acute ischaemic stroke is effective and safe and is
recommended by the American Heart Association/
American Stroke Association guidelines.1 However,
few reports have examined the risk of endothelial injury from thrombectomy.2 We present a case
of endothelial injury possibly due to mechanical
thrombectomy that caused repeated occlusion of
the treated vessel.

Case presentation

© BMJ Publishing Group
Limited 2019. No commercial
re-use. See rights and
permissions. Published by BMJ.
To cite: Hidaka M,
Yamaguchi S, Koyanagi Y,
et al. BMJ Case Rep
2019;12:e228937.
doi:10.1136/bcr-2018228937

A 92-year-old woman developed sudden consciousness disturbance, aphasia and right hemiparesis. She
had taken edoxaban (30 mg/day) for atrial fibrillation but discontinued it because of haemorrhagic
cystitis 2 months prior. The onset-to-door time
was 102 min. Neurological examination revealed
impaired consciousness (Glasgow Coma Scale
(GCS) score was 11/15, E4V1M6), global aphasia,
right hemiparesis that included the face (manual
muscle test score: upper extremity, 1/5 and lower
extremity, 1/5) and right side sensory disturbance.
The National Institutes of Health Stroke Scale
(NIHSS) score was 36.

Investigations

A hypercoagulable state was suspected because of
elevated D-dimer and fibrin degradation product
levels (6.9 and 13.7 µg/mL, respectively). Electrocardiography revealed atrial fibrillation, and no
thrombus was observed on transthoracic echocardiography. Carotid echocardiography revealed
decreased end-diastolic flow of her left common
carotid artery and suggested occlusion of the left
middle cerebral artery (MCA) or internal carotid
artery (ICA).3 CT, underwent 111 min from onset,
revealed a slightly low density at the left temporal
pole and hyperdense MCA sign on the left side. The
Alberta Stroke Programme Early CT score was 9.

Treatment

We started intravenous tissue plasminogen activator
at 137 min after onset, but her symptoms did not
change. Endovascular treatment was initiated, and
complete occlusion of the left MCA was confirmed
(figure 1A). We placed a 9-Fr Optimo catheter
(Tokai Medical Products, Aichi, Japan) at the
cervical portion of the left ICA and conducted clot
retrieval with direct aspiration first-pass technique
(ADAPT).4 We placed a 5-MAX ACE Penumbra
catheter (Penumbra, CA, USA) at the proximal
side of the thrombus and commenced aspiration.
However, the catheter slipped into the M2 portion
of the left MCA; nevertheless, red thrombus was
retrieved and complete recanalisation was achieved
(thrombolysis in cerebral infarction (TICI) grade 3;
figure 1B). No neurological change was observed
after the first mechanical thrombectomy. In our
hospital, We conduct MRI/MR angiography (MRA)
after mechanical thrombectomy as part of protocol
for investigating the stroke volume, intracranial
haemorrhage and the treated vessels. MRI just after
thrombectomy revealed a minimum high-intensity
area on diffusion-weighted images. However, MRA
revealed narrowing of the treated vessel (figure 2A).
Repeat MRA 10 min later revealed occlusion of the
left MCA (figure 2B). A second endovascular treatment was attempted.

Outcome and follow-up

Cerebral angiography revealed occlusion of the left
MCA at the M1 portion, 4 mm distal to the initial
occlusion site (figure 3A). We repeated the initial
procedure. A 5-MAX ACE Penumbra catheter
was carefully advanced to the proximal side of the

Hidaka M, et al. BMJ Case Rep 2019;12:e228937. doi:10.1136/bcr-2018-228937

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Reminder of important clinical lesson

Figure 1 (A) Left ICA angiography shows occlusion of left MCA.
(B) After first mechanical thrombectomy. Left ICA angiography shows
favourable recanalisation of left MCA (thrombolysis in cerebral
infarction Grade 3). ICA, internal cerebral artery; MCA, middle cerebral
artery.
thrombus to prevent device slipping. The thrombus was removed
using ADAPT, and complete recanalisation (TICI grade 3) was
achieved again (figure 3B). However, cerebral angiography
10 min after the second treatment again revealed narrowing of
the left MCA at the M1 portion (figure 3C). No findings indicated dissection. Endothelial injury may have occurred when the
catheter slipped into the left M2, leading to repeated thrombus
formation. We administered ozagrel 80 mg, aspirin 100 mg and
clopidogrel 75 mg. After 13 min, cerebral angiography revealed
complete left MCA recanalisation (figure 3D).
We continued ozagrel, aspirin and clopidogrel for 5 days.
MRA on hospital day 6 revealed no MCA reocclusion (figure 4).
Eventually, edoxaban (30 mg/day) and clopidogrel (75 mg/day)
were chosen for secondary prevention. She recovered from her
consciousness disturbance and aphasia (GCS score was 15/15,
E4V5M6), though she remained right hemiparetic after re-treatment. NIHSS on her 21st day of hospitalisation was 26. She was
transferred to a rehabilitation hospital for further treatment.

Discussion

Factors contributing to thrombogenesis in recanalised vessels
after mechanical thrombectomy for acute ischaemic stroke
include endothelial injury, release of tissue factors, platelet activation, adhesion and aggregation.5 In our case, endothelial injury
may have occurred during thrombectomy, leading to recurrent
occlusion. Abraham et al analysed endothelial injury through
endovascular treatment using MRI. They assessed six patients’
MRI 24 hours after mechanical endovascular treatment with
stent type devices. All these patients showed signal enhancement

Figure 2 (A) MRA after first endovascular treatment; it reveals poor
visualisation of the MCA. (B) 13 min later, MRA shows the reocclusion of
left MCA. MCA, middle cerebral artery; MRA, MRA angiography.
2

Figure 3 (A) The second mechanical thrombectomy. Left ICA
angiography shows occlusion of left MCA at M2 portion. (B) Just after
second mechanical thrombectomy. Angiography of the left ICA shows
recanalisation of left MCA (thrombolysis in cerebral infarction Grade
3). (C) Angiography after 10 min interval shows mural thrombus.
(D) Angiography after administration of antiplatelet drugs shows
improvement of the mural thrombus. ICA, internal cerebral artery; MCA,
middle cerebral artery.

of the vessel wall which suggested endothelial injury. So, we are
afraid that the incidence of such event may not be rare.2
Gory et al found that both stent and aspiration devices might
cause endothelial denudation and medial oedema.6 However,
aspiration devices were less likely to cause endothelial denudation and intramural thrombus formation. They speculated that

Figure 4 MR angiography after second thrombectomy and
administration of antiplatelet drugs reveals favourable visualisation of
left MCA. MCA, middle cerebral artery.
Hidaka M, et al. BMJ Case Rep 2019;12:e228937. doi:10.1136/bcr-2018-228937

BMJ Case Rep: first published as 10.1136/bcr-2018-228937 on 26 August 2019. Downloaded from http://casereports.bmj.com/ on November 4, 2019 at Flower/Sprecher Library College
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Reminder of important clinical lesson

aspiration devices had a smaller contact area within the vessel
and were less likely to cause endothelial injury than stent devices.
Teng et al reported that the pattern and severity of endothelial
injury differed depending on the endovascular treatment device.7
They conducted mechanical thrombectomy using various types
of devices for different vessel sizes, and concluded that aspiration
devices caused least endothelial injury and that the narrower the
vessel, the more severe the endothelial injury.
In our case, endothelial injury probably occurred because the
catheter slipped into the M2 portion, which was smaller than the
device diameter. We should have carefully placed 5-MAX ACE
Penumbra catheter not to slip to the M2 portion.
Ozagrel, a selective thromboxane A2 synthase inhibitor, was
administered intravenously. Therapy with ozagrel, aspirin and
clopidogrel was definitely effective for resolving thrombotic
occlusion in this case.
Repeated occlusion of a treated vessel in this case was probably
due to endothelial injury after mechanical thrombectomy for an acute
ischaemic stroke. This is an uncommon but serious adverse event,
but thrombosis may occur from endothelial injury after mechanical

Learning points
►► We report a case of repeated occlusion of a treated vessel

after mechanical thrombectomy for acute ischaemic stroke.
The endothelial injury caused by thrombectomy may
have triggered thrombotic occlusion, which resolved with
antiplatelet agents.
►► Mechanical thrombectomy may cause endothelial injury and
thrombotic occlusion of a treated vessel.
►► The occurrence do not differ owing to the device type.
►► Antiplatelet agents may be effective in such case.

thrombectomy regardless of the type of device. Selecting the proper
device size to avoid endothelial injury is important.
Contributors Conception and design, acquisition of data or analysis and
interpretation of data: SA and MH. Drafting the article or revising it critically
for important intellectual content: MH, YK and SY. Final approval of the version
published: SY. Agreement to be accountable for the article and to ensure that all
questions regarding the accuracy or integrity of the article are investigated and
resolved: MH, SA, YK and SY.
Funding The authors have not declared a specific grant for this research from any
funding agency in the public, commercial or not-for-profit sectors.
Competing interests None declared.
Patient consent for publication Next of kin consent obtained.
Provenance and peer review Not commissioned; externally peer reviewed.

References

1 Powers WJ, Derdeyn CP, Biller J, et al. 2015 American Heart Association/American
Stroke Association Focused Update of the 2013 Guidelines for the Early Management
of Patients with Acute Ischemic Stroke Regarding Endovascular Treatment: A Guideline
for Healthcare Professionals from the American Heart Association/American Stroke
Association. Stroke 2015;46:3020–34.
2 Abraham P, Scott Pannell J, Santiago-Dieppa DR, et al. Vessel wall signal enhancement
on 3-T MRI in acute stroke patients after stent retriever thrombectomy. Neurosurg
Focus 2017;42:E20.
3 Yasaka M, Omae T, Tsuchiya T, et al. Ultrasonic evaluation of the site of carotid axis
occlusion in patients with acute cardioembolic stroke. Stroke 1992;23:420–2.
4 Turk AS, Spiotta A, Frei D, et al. Initial clinical experience with the ADAPT technique:
a direct aspiration first pass technique for stroke thrombectomy. J Neurointerv Surg
2014;6:231–7.
5 Becker R. Dynamics of coronary thrombolysis and reocclusion. Clin Cardiol
1997;20:2–5.
6 Gory B, Bresson D, Kessler I, et al. Histopathologic evaluation of arterial wall response
to 5 neurovascular mechanical thrombectomy devices in a swine model. AJNR Am J
Neuroradiol 2013;34:2192–8.
7 Teng D, Pannell JS, Rennert RC, et al. Endothelial trauma from mechanical
thrombectomy in acute stroke: in vitro live-cell platform with animal validation. Stroke
2015;46:1099–106.

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Hidaka M, et al. BMJ Case Rep 2019;12:e228937. doi:10.1136/bcr-2018-228937

3

BMJ Case Rep: first published as 10.1136/bcr-2018-228937 on 26 August 2019. Downloaded from http://casereports.bmj.com/ on November 4, 2019 at Flower/Sprecher Library College
ofVeterinary Medicine. Protected by copyright.

Reminder of important clinical lesson