Clin Neuroradiol (2013) 23:225–229
DOI 10.1007/s00062-012-0172-z

Correspondence

Analysis of Reserve Capacity and Subsequent Stenting in a Case
of Subacute Occlusion of the Internal Carotid Artery
K. Kallenberg · J. Rühlmann · J. Baudewig · J. Larsen ·
S. Gröschel · P. Dechent · A. Kastrup · M. Knauth

Received: 10 May 2012 / Accepted: 13 August 2012 / Published online: 8 September 2012
© The Author(s) 2012. This article is published with open access at Springerlink.com

Introduction
In stroke patients, an acute thrombotic occlusion of an
internal carotid artery (ICA) is a poor predictor for clinical
outcome [1]. It has occasionally been managed by carotid
endarterectomy [2] (CEA) or percutaneous transluminal
angioplasty (PTA) with [3] or without [4] stent protection
(carotid angioplasty and stenting, CAS). On the other hand,
a chronic thrombotic occlusion (CTO) of the ICA may be
treated successfully by external–internal carotid artery (EC–
K. Kallenberg, M.D. () · Dr. med. J. Rühlmann ·
Dr. J. Baudewig
Department of Neuroradiology, MR-Research in Neurology
and Psychiatry, University Medical Center Göttingen
Robert-Koch-Str. 40, 37099 Göttingen, Germany
e-mail: kai.kallenberg@med.uni-goettingen.de
Dr. J. Baudewig
Department of Diagnostic Radiology,
Christian-Albrechts-University Kiel, Kiel, Germany
Dr. med. J. Larsen
Department of Radiology, Evangelisches Krankenhaus
Göttingen-Weende, Göttingen, Germany
Dr. med. S. Gröschel
Department of Psychiatry and Psychotherapy, University Medical
Centre, Mainz, Germany
PD Dr. P. Dechent
Department of Cognitive Neurology, MR-Research in Neurology
and Psychiatry, Universitymedicine Göttingen, Göttingen, Germany
Prof. Dr. med. A. Kastrup
Department of Neurology,
Klinikum Bremen-Mitte, Bremen, Germany
Prof. Dr. med. M. Knauth
Department of Neuroradiology,
University Medical Center Göttingen, Göttingen, Germany

IC) bypass surgery [5, 6]. However, EC–IC together with
best medical treatment (BMT) does not reduce the risk of
an ipsilateral stroke compared with BMT alone [7]. In addition, there have also been recent reports on CAS in patients
with symptomatic CTO [8, 9] and CAS has a serious role in
patients with high operative risk.
We herein report on the diagnostic work-up and subsequent therapeutic management of a patient with symptomatic thrombotic occlusion of the left extracranial ICA and a
pre-existing occlusion of the contralateral ICA [10].
Case Report
A 65-year-old male with multiple cardiovascular risk factors presented with dysarthria and central right-sided facial
palsy following an episode of syncope. The patient was
admitted to our stroke unit where he experienced blood
pressure-dependent right-sided weakness and sensorimotor
aphasia, initially controllable by conservative therapy.
Pre-Interventional Assessment
Computed tomography (CT)-angiography (CTA; Aquilion,
Toshiba Medical Systems Europa, Zoetermeer, Niederlande) showed bilateral ICA occlusion and the magnetic
resonance (MR) scan on a 3Tesla MR-system (TIM TRIO®,
Siemens Medical Solutions, Erlangen, Germany) demonstrated multiple chronic microvascular lesions bilaterally on
T2-weighted images. Diffusion-weighted imaging (DWI)
revealed acute infarctions in a watershed distribution with
additional significant prolongation of both the mean transit
time (MTT) and time to peak (TTP) in the left hemisphere.
Conventional catheter angiography (digital subtraction
angiography, DSA) finally confirmed the diagnosis of bila-

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hemisphere, mainly in the middle cerebral artery (MCA)
territory, thus indicating a marked reduction of reserve
capacity (Fig. 2).
Intervention

Fig. 1 Catheter angiography (DSA) demonstrates complete occlusion
of the left internal carotid artery

teral ICA occlusion (Fig. 1) and revealed collateralisations
via the ophthalmic arteries as well as via vertebro-basilar
pathways. Importantly, origin and subsequent course of the
left external carotid artery (EC) were found to be entirely
normal and an EC–IC bypass was considered accordingly.
Given the patient’s recurrent symptoms, assumingly of
hemodynamic origin, an urgent intervention was required.
To further support such a decision, a Blood Oxygenation
Level Dependent MR scan was obtained (Fig. 2) to evaluate
the patient’s cerebrovascular reserve capacity (CRV) [11,
12]: The experimental set-up had previously been approved
by the local ethics committee and included a bottled carbon
dioxide (CO2) source and a dedicated magnetic resonance
imaging (MRI) patient-monitoring device (GE Medical
Systems Information Technologies, Freiburg, Germany).
The patient was prepared with a conventional facial nonrebreathing mask and a gas bag connected for a 3 min-CO2
challenge to induce hypercapnia.
The analysis of BOLD signal intensity changes was
performed using an in-house software package (Brainshow [13]). The BOLD response was diminished in the left

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The patient was treated with 100 mg aspirin p. o. before
admission. Then, he was given an additional 75 mg clopidogrel p. o. and because of the fluctuating symptoms the
aspirin dosage was raised to 300 mg and also low-dose
heparin was administered.
Eight days following the initial event, the patient’s symptoms suddenly deteriorated irrespective of maximum conservative therapy. Since emergency EC–IC bypass surgery
was not possible logistically, the patient agreed to attempt
a neuroendovascular revascularisation. Written informed
consent was obtained and stent-protected CAS performed.
In addition to the established anticoagulation, further heparin was given via intravenous infusion during the procedure
(activated clotting time, ACT = 250 − 300 s).
Selective left common carotid artery catheterisation was
performed according to standard aseptic technique using
a guide-wire (Terumo, Tokyo, Japan) and a 7F guide catheter (Mach 1™, Boston Scientific, Natick/MA, USA). A
microcatheter (FastTracker 18™, Boston Scientific, Natick/
MA, USA) with a 0.014-in guide-wire (Synchro 14; Boston Scientific, Natick/MA, USA) was utilised to carefully
negotiate the lumen of the occluded vessel under biplanar
fluoroscopic control to a level beyond the occlusion; intraluminal position confirmed by microcatheter series. A 7/40
Carotid Wallstent™ Monorail™-System (Boston Scientific,
Natick/MA, USA) was then deployed, followed by balloon
angioplasty using a 5/20 Sterling™ balloon catheter (Boston Scientific, Natick/MA, USA) at an inflation pressure of
8 bar.
The final angiogram series demonstrated a small intimal
flap distal to the stent indicating a minor dissection which
was considered to be adequately treated by the present anticoagulation regimen. However, we attributed the very small
post-interventional diameter of the extracranial ICA primarily to the previous collapse (Figs. 3 and 4). The vessel diameter was monitored by duplex-ultrasound and normalised
within 48 h. The control CT-angiography after 1 week confirmed a patent vessel diameter and the very small intimal
flap which finally healed without any additional interventional treatment.
The patient’s subsequent course was uneventful. His preinterventional neurological symptoms subsided. Follow-up
MRI showed no new infarct. Cerebral perfusion as well as
CRV (Fig. 2) improved markedly. A follow-up CTA examination of the carotid arteries at 3 months revealed persistence of excellent luminal reconstruction without recurrent
stenosis.

Analysis of Reserve Capacity and Subsequent Stenting in a Case of Subacute Occlusion of the Internal Carotid Artery

227

Fig. 2 Representative supratentorial slices prior to (left)
and after (right) carotid artery
stenting show a significant
difference in hypercapniainduced BOLD signal
intensity changes between
the hemispheres: an initial
restriction (left) and the subsequent improvement (right)
of cerebrovascular reactivity
can be clearly seen in the left
MCA territory

Fig. 3 Catheter angiography
images showing successful
left internal carotid artery
(LCI) revascularisation with
anterograde filling of MCA
branches after stenting and
stent position (un-subtracted
image)

After the neurointerventional procedure the anticoagulation regimen was maintained for 1 week and then reduced
to 100 mg aspirin and 75 mg clopidogrel for 3 months. The
patient is on 100 mg aspirin since.

Discussion
In the setting of acute or chronic carotid artery occlusion,
cerebral ischemia may principally result from either embolic
occlusion with resulting territorial ischemia or from reduced

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Fig. 4 The post-interventional DSA image in frontal view shows the
filling of the ipsilateral MCA (image quality is considerably diminished as the patient was only minimally sedated for the procedure and
became progressively agitated)

regional perfusion with consequent hemodynamically distributed infarcts. While the value of thrombolysis and fibrinolysis in the acute setting has been shown to be beneficial
[14], the mechanism underlying the acute deterioration in
our case was rather due to hypoperfusion rather than thromboembolism. EC–IC bypass has been reported in a selected
group of patients with poor reserve capacity when CEA was
not possible [6]. In our case, EC–IC bypass appeared appropriate but was not applicable because of the acuteness of the
patient’s deterioration. Paty et al. [15] reported on success
rates of CEA of the order of 30 % when performed within
14 days after the onset of symptoms. Furthermore, successful CAS [16] and stent-assisted revascularisation of intracranial vessels [17] in a subacute stage had been reported.

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K. Kallenberg et al.

In patients with co-existing conditions leading to a higher
operative risk, CAS is not inferior to CEA [10]. However,
at this particular time, there is no scientific evidence for the
sufficient safety of endovascular revascularisation of totally
occluded ICAs.
Measurement of CRV by the means of Xenon-CT has
been suggested as a surrogate parameter when selecting
patients for cerebrovascular therapy [18]. Alternatively,
the applicability of CO2 exposure-induced hypercapnia in
combination with BOLD-contrast functional MR has been
demonstrated [11, 19, 20]. Considering our patient’s symptoms and his restricted cerebrovascular reserve, an attempt
of revascularisation was indicated.
Taking the risk of distal embolisation into account, a
blood flow manipulation with proximal balloon occlusion
of the common carotid artery was discussed before the intervention but not taken into account because it would not have
added any benefit as long as external artery branches were
still open [21]. Furthermore, it would have led to a flow
reversal in the ophthalmic artery with the threat of a steal
phenomenon and unpredictable consequences. The only
double-balloon device available in our department has a
very small lumen which seemed inappropriate in the present
setting. In addition, the pre-operative work-up for the EC–
IC bypass demonstrated a substantial contribution from the
external carotid artery to the brain perfusion. Any further
reduction of arterial input should be avoided under those
precarious circumstances. The contrast injection through
the microcatheter showed no relevant thrombus load in
the ICA distal to the occlusion—in this case the procedure
would have had to be adjusted, e.g. applying vacuum thrombectomy [22, 23].
In the past, several reports of reperfusion injury following recanalisation by either CEA [24–26] or CAS [27, 28]
have led to a very careful selection of patients, especially in
cases with prolonged ischemia. For this reason, initial therapy in our patient comprised medical therapy with anticoagulation as well as blood-pressure elevation only. However,
this approach did not yield a satisfactory result: symptoms
were fluctuating and aggravated over time. Following further deterioration with sudden onset of aphasia and hemiparesis, an ultima ratio decision was therefore made to attempt
neuroendovascular revascularisation.
CAS in subacute ICA occlusion is feasible and may lead
to a favourable outcome but should be restricted to carefully
selected cases. The non-invasive assessment of cerebrovascular CO2 reactivity using BOLD-contrast MRI might provide valuable information in this setting.
Acknowledgements The authors (K. Kallenberg, J. Baudewig and P.
Dechent) were supported by the Volkswagen Stiftung (Grants ZN1635
and ZN 2193).

Analysis of Reserve Capacity and Subsequent Stenting in a Case of Subacute Occlusion of the Internal Carotid Artery
Financial Disclosure The authors (K. Kallenberg and M. Knauth)
state the following financial disclosures: Speakers Bureau (K. Kallenberg [Acandis, Pforzheim/Germany] and M. Knauth [Penumbra,
Alameda/USA; Siemens Healthcare, Erlangen/Germany; Acandis,
Pforzheim/Germany; Codman, Norderstedt/Germany]).
Conflict of Interest The authors declare that there is no actual or
potential conflict of interest in relation to this article.
Open Access This article is distributed under the terms of the Creative
Commons Attribution License which permits any use, distribution, and
reproduction in any medium, provided the original author(s) and the
source are credited.

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