- Email: [email protected]
Endovascular Treatments in Combination with Extracranial-Intracranial Bypass for Complex Intracranial Aneurysms
Accepted Manuscript Endovascular treatments in combination with extracranial-intracranial bypass for complex intracranial aneurysms Kenichi Sato, M.D., Hidenori Endo, M.D., Miki Fujimura, M.D., Toshiki Endo, M.D., Yasushi Matsumoto, M.D., Hiroaki Shimizu, M.D., Teiji Tominaga, M.D. PII:
S1878-8750(18)30416-9
DOI:
10.1016/j.wneu.2018.02.143
Reference:
WNEU 7558
To appear in:
World Neurosurgery
Received Date: 3 December 2017 Revised Date:
21 February 2018
Accepted Date: 23 February 2018
Please cite this article as: Sato K, Endo H, Fujimura M, Endo T, Matsumoto Y, Shimizu H, Tominaga T, Endovascular treatments in combination with extracranial-intracranial bypass for complex intracranial aneurysms, World Neurosurgery (2018), doi: 10.1016/j.wneu.2018.02.143. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT 1
Endovascular treatments in combination with extracranial-intracranial bypass for complex intracranial aneurysms
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Kenichi Sato, M.D., 1 Hidenori Endo, M.D., 2 Miki Fujimura, M.D., 3 Toshiki Endo,
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M.D., 3 Yasushi Matsumoto, M.D., 1 Hiroaki Shimizu, M.D., 4 Teiji Tominaga, M.D. 2
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Department of Neuroendovascular Therapy, Kohnan Hospital, Sendai, Japan
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Department of Neurosurgery, Tohoku University Graduate School of Medicine,
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Sendai, Japan 3
Department of Neurosurgery, Kohnan Hospital, Sendai, Japan
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Department of Neurosurgery, Akita University Graduate School of Medicine, Akita,
Japan
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Corresponding Author: Kenichi Sato, M.D., Ph.D.
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Department of Neuroendovascular Therapy, Kohnan Hospital
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4-20-1, Nagamachi-minami, Taihaku-ku, Sendai, 982-8523, Japan
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Telephone: 81-22-248-2131
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Fax: 81-22-248-1966
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Email: [email protected]
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Key Words: bypass surgery, cerebral aneurysm, cerebral revascularization,
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endovascular treatment, fusiform aneurysm, large aneurysm
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Abbreviations:
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BTO: balloon test occlusion
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ECA: external carotid artery
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ICA: internal carotid artery
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MCA: middle cerebral artery
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mRS: modified Rankin Scale
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OA: occipital artery
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PCA: posterior cerebral artery
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PICA: posterior inferior cerebellar artery
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SPECT: single-photon emission computed tomography
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SCA: superior cerebellar artery
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STA: superficial temporal artery
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ACCEPTED MANUSCRIPT Abstract
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Objective: Although most intracranial aneurysms can be treated with microsurgery or
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endovascular procedure alone, a subset of aneurysms may require a combined
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approach. The purpose of this study was to assess the efficacy of endovascular
5
interventions combined with bypass surgery for the treatment of complex intracranial
6
aneurysms.
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Methods: We retrospectively reviewed medical records from a prospectively
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maintained patient database to identify patients who underwent endovascular
9
treatment of an intracranial aneurysm at our institutes from 2007 to 2017. We
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recruited patients who received a pre-planned combination of endovascular treatment
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and extracranial-intracranial bypass surgery.
Results: Forty-four patients (44 aneurysms) were treated with a combined approach.
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Twenty-four patients presented with subarachnoid hemorrhage. Treatment strategies
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included endovascular parent artery occlusion with the bypass surgery to restore
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cerebral blood flow (n=12), endovascular trapping with bypass surgery to isolate
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incorporated branches (n=12), and intra-aneurysmal coil embolization with bypass
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surgery to isolate incorporated branches (n=20). During a mean period of 35.6 months,
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follow-up catheter angiography was performed in 35 of 44 patients (79.5%) and demonstrated complete aneurysm obliteration in 29 patients (82.9%) and bypass
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patency in 33 (94.3%). The postoperative aneurysm-related mortality and morbidity
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rates were 6.8% and 13.6%, respectively.
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Conclusion: Combined endovascular and surgical bypass procedures are useful for
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the treatment of complex intracranial aneurysms when conventional surgical or
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endovascular techniques are not feasible and show acceptable rates of morbidity and
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mortality.
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ACCEPTED MANUSCRIPT Introduction
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Patients with large and giant saccular or fusiform intracranial aneurysms commonly
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manifest mass effect-related symptoms, ischemic stroke secondary to occlusion of
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involving perforating branches or thromboembolism, and subarachnoid hemorrhage.1
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Because the natural history of these aneurysms leads to disastrous clinical outcomes,
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it is widely agreed that they should not be left untreated.2-5
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The treatment of these complex intracranial aneurysms may be challenging in spite
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of advances in endovascular procedures and the introduction of refined microsurgical
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techniques.6-9 Large and giant saccular aneurysms may have wide necks with major
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branches or perforating arteries incorporated at the neck or the dome, atherosclerotic
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or calcified walls, and a partially thrombosed lumen. Fusiform aneurysms have no
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neck at all, as the entire wall of the involved arterial segment is pathologically
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dilated, and the lumen may be partially thrombosed. Thus, these lesions are not
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amenable to conventional surgical treatments.3,10,11 Even the use of advanced
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endovascular devices such as flow diverters may result in high complication rates and
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poor angiographic results, especially in posterior circulation aneurysms.12
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When conventional surgical management is not feasible, complex aneurysms can be managed by combining endovascular techniques and microsurgical revascularization, although a limited number of studies describing this combined
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approach to aneurysm treatment have been published.13-20 In this study, we
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retrospectively reviewed our experience with combined endovascular treatment and
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extracranial-intracranial bypass surgery. The purpose of this study was to evaluate the
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efficacy and technical safety of endovascular procedures combined with bypass
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surgery in complex aneurysms that were not amenable to conventional approaches.
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Methods 4
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We retrospectively reviewed medical records from a prospectively maintained patient
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database to identify all patients who underwent endovascular treatment of an
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intracranial aneurysm at our institutes from May 2007 to June 2017. We recruited
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those who received a combination of endovascular treatment and
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extracranial-intracranial bypass surgery. Those whose bypass procedure was not
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pre-planned, e.g., those who underwent rescue bypass surgery for ischemic
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complications after endovascular treatment, were excluded. We analyzed each
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patient’s hospital course and perioperative outcome. Long-term clinical follow-up was
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attempted for each patient through chart review, patient telephone interview, or both.
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The institutional review board approved this retrospective study and informed consent
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was obtained for all patients in written form as well as orally.
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Surgical management
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Aneurysm treatment decisions were made on an individual basis in conjunction with
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our multidisciplinary team. Preoperative surgical planning, including the bypass type
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and whether to perform vessel occlusion or aneurysm embolization, was based on the
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angiographic findings. Treatment strategies included the following:
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Type A: endovascular parent artery occlusion with bypass surgery to restore cerebral
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blood flow (Figure 1)
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Type B: endovascular trapping with bypass surgery to isolate branches incorporated
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into the aneurysm (Figure 2)
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Type C: intra-aneurysmal coil embolization with bypass surgery to isolate branches
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incorporated into the aneurysm (Figure 3)
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The type of bypass surgery (single, double, or high-flow bypass using the
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saphenous vein) was based on the results of preoperative balloon test occlusion
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(BTO) using single-photon emission computed tomography (SPECT) or 5
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internal carotid artery (ICA) aneurysms.22 Otherwise, we preferred to use a single
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bypass with the superficial temporal artery (STA) or the occipital artery (OA) as the
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donor to isolate vascular branches incorporated into the aneurysm (types B and C).
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All surgical treatments were performed under general anesthesia. Patients with
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unruptured aneurysms were prescribed 100mg aspirin three days before bypass
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surgery. Bypass patency was assessed intraoperatively using direct blood flow
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measurement by Doppler ultrasound and indocyanine green video angiography and
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confirmed by catheter angiography before beginning the endovascular procedure.
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Patients were given antiplatelet agents (300mg clopidogrel and 200mg aspirin)
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through a nasogastric tube immediately after arterial punctures for endovascular
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treatment. Postoperatively, dual antiplatelet therapy (75mg/day clopidogrel and
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100mg/day aspirin) was maintained for six months and then changed to clopidogrel
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monotherapy (75 mg/day) for an additional six months. The activated coagulation
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time was monitored from the beginning of the endovascular procedure and
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maintained at a target value between 200 and 250 seconds. A dose of heparin (80
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IU/kg) was injected intravenously followed by the administration of 16 IU/kg of
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heparin per hour. Heparin neutralization was routinely achieved by the administering
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50 mg protamine sulfate at the end of endovascular procedures. A computed
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tomography brain scan was performed immediately after each procedure for early
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detection of intracranial hemorrhagic complications.
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Outcomes
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Angiographic findings were evaluated according to the Raymond classification
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immediately after treatment and at follow-up.23 Postoperative angiographic follow-up
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was performed at 6, 12, and 24 months, and as needed. Angiographic recurrence was
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defined as any worsening of the Raymond classification or enlargement of the 6
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residual aneurysm. Bypass patency was also assessed angiographically. When an
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angiographic recurrence was considered progressive or large enough to be embolized
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again, retreatment was planned.
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Neurological outcomes were assessed using the modified Rankin Scale (mRS) score. Perioperative death and major stroke (mRS>2) were defined as
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procedure-related mortality and morbidity, respectively. Each patient was evaluated
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using mRS score at follow-up, and any worsening was recorded.
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Results Patient and Aneurysms Characteristics
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During the study period, 1,683 aneurysms were treated using endovascular techniques.
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Of these, 44 aneurysms (2.6%) in 44 patients (male, n=12; mean age, 59.9 years; age
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range, 29-82 years) received endovascular treatment combined with
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extracranial-intracranial bypass surgery. Clinical presentations included subarachnoid
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hemorrhage (n=24), cranial nerve palsy (n=5), headache (n=3), brainstem
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compression (n=3), hydrocephalus (n=2), and no symptoms (n=7). Aneurysms were
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located in the anterior circulation (n=15, 34.1%) and posterior circulation (n=29,
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65.9%). Twenty-seven aneurysms had saccular morphology, including 18 large or
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giant aneurysms. Four aneurysms had been previously treated elsewhere with coil
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embolization with or without stents (Table 1)
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Surgical Treatment
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Table 2 summarizes the surgical procedures performed. We used the type A strategy
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in 12 patients (27.3%), type B in 12 (27.3%), and type C in 20 (45.5%). The bypass
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procedure was followed by endovascular treatment in 40 patients (90.9%). In four
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patients with a ruptured vertebral arterial dissection involving the origin of the
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posterior inferior cerebellar artery (PICA), we performed endovascular proximal
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occlusion in the acute stage, and then trapped the dissected vertebral artery with
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OA-PICA bypass surgery in the chronic stage. The interval between the bypass
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surgery and endovascular treatment was within 24 hours in 32 patients (72.7%),
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within one week in 7 (15.9%), and greater than one week in 5 (11.4%). There were 52 bypass procedures performed in the 44 patients. Three STA-middle
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cerebral artery (MCA) bypasses were a double bypass in which both frontal and
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parietal branches of the STA were used. A double bypass procedure involving
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STA-posterior cerebral artery (PCA) and STA-superior cerebellar artery (SCA)
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bypasses was performed in three patients. Four patients without tolerance to ICA
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occlusion underwent external carotid artery (ECA)-MCA bypass using a saphenous
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vein graft.
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There were 49 endovascular procedures including parent artery occlusion (n=12), aneurysm trapping (n=12) and intra-aneurysmal coil embolization (n=25). Five
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patients with ICA aneurysms underwent simultaneous intra-aneurysmal coiling and
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parent artery occlusion. Stent-assisted intra-aneurysmal coil embolization was
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performed in 15 patients (34.1%). Eight patients (18.2%) required repeated
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endovascular treatments, including additional coil placement in a recanalized
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aneurysmal sac in five, and parent artery occlusion in three.
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Angiographic Outcomes
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Angiographic results are summarized in Table 3. Angiograms obtained immediately
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after the procedures revealed complete aneurysm obliteration in 29 patients (65.9%),
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a residual neck in 4 (9.1%), and a residual aneurysm in 11 (25.0%). Angiographic
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follow-up at 14.9 ± 3.2 months after the treatment was available in 35 patients
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(79.5%). We achieved complete aneurysm obliteration by parent artery occlusion or
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trapping with coils in 6 patients (13.6%), thus obviating the need for follow-up
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catheter angiography. Three patients (6.8%) died within six months of treatments. In 8
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9 of 35 patients (25.7%), follow-up angiograms revealed further thrombosis of the
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aneurysmal sac. The final results included 29 (82.9%) complete occlusions, 3 (8.6%)
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residual necks, and 3 (8.6%) residual aneurysms.
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Follow-up angiograms revealed a satisfactory bypass patency in 33 of 35 patients (94.3%). One patient with a ruptured vertebral artery dissection underwent
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endovascular trapping of the dissection in combination with right OA-PICA bypass.
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Diffusion-weighted images performed the following day demonstrated acute
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infarction in the right cerebellar hemisphere, and magnetic resonance angiography did
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not show bypass patency. Another patient suffered from severe brainstem infarction
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due to progressive thrombosis after bilateral vertebral artery coil occlusion with the
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right STA-PCA and STA-SCA bypasses and isolation of the left PCA for a large
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symptomatic basilar bifurcation aneurysm. Her right STA-PCA anastomoses, as well
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as the treated aneurysm, had progressively thrombosed after the left PCA was
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isolated.
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Clinical Outcomes
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Table 4 shows the mRS scores for each treatment strategy. Overall, a good outcome
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(mRS score of 0-2) was observed in 34 patients (77.3%), and a poor outcome (mRS
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score of 3-6) was observed in 10 (22.7%). The mean length of postoperative
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follow-up for all patients was 35.6 ± 4.6 months.
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Five patients (11.4%) died in the follow-up period, including 3 (6.8%) with
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aneurysm related complications. One patient with an unruptured PICA aneurysm
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treated with intra-aneurysmal coil embolization combined with OA-PICA bypass died
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in the postoperative period due to an acute subdural hematoma. One patient with a
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giant basilar trunk aneurysm died of subarachnoid hemorrhage three months after
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treatment. One patient with a ruptured giant supraclinoid ICA aneurysm treated with parent artery coil occlusion and double STA-MCA bypass died because of severe 9
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cerebral vasospasm. Two patients died of medical complications, including cardiac
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failure (n=1) and pneumonia (n=1). Seven patients (15.9%) had a lower mRS score in the follow-up period than they
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had preoperatively, including 6 (13.6%) patients with aneurysm related complications .
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Of these patients, three (6.8%) had permanent deficits as a result of treatment-related
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complications including two with a cerebral infarction and one with a cerebral
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contusion. Two patients with a symptomatic large basilar bifurcation aneurysm
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underwent endovascular treatment with bypasses, which resulted in residual filling of
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the aneurysm. These patients presented with a disturbance of consciousness
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postoperatively due to brainstem compression by the treated aneurysm.
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Illustrative Cases
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Case 1 (type A strategy)
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A 49-year-old woman presented with subarachnoid hemorrhage (WFNS grade
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due to a ruptured fusiform aneurysm at the supraclinoid segment of the left ICA.
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Cerebral angiography revealed the size of the aneurysm was 6.8 × 6.7 × 5.9 mm
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and the left ophthalmic artery originated from the dome of the aneurysm (Figure 4A).
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She underwent SPECT-based BTO, which demonstrated that the left cerebral
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hemisphere blood flow was 65% lower than the flow on the contralateral side and
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retrograde filling of the aneurysm via the left ophthalmic artery during the occlusion
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of the left ICA. High-flow bypass was performed immediately followed by
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endovascular trapping of the fusiform aneurysm (Figure 4B). Postoperative
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angiography showed the complete disappearance of the aneurysm and satisfactory
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bypass graft patency (Figure 4C – 4F). The patient returned to normal daily activities
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without any neurological deficits.
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Case 2 (type B strategy) 10
ACCEPTED MANUSCRIPT A 58-year-old woman experienced the sudden onset of a severe headache without
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subarachnoid hemorrhage. Magnetic resonance imaging detected a left intracranial
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vertebral artery dissection (Figure 5A). The left PICA was arising from the
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aneurysmal dilatation. She was managed conservatively, but the dissecting aneurysm
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gradually enlarged. We performed endovascular trapping of the dissecting aneurysm
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with OA-PICA bypass (Figure 5B). The patient’s postoperative course was
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uneventful. Cerebral angiograms obtained six months after treatment demonstrated
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complete disappearance of the dissecting aneurysm and satisfactory bypass patency
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(Figure 5C – 5F).
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Case 3 (type C strategy)
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A 64-year-old woman presented with subarachnoid hemorrhage (WFNS grade
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due to a ruptured 17.6-mm-diameter basilar bifurcation aneurysm (Figure 6A). She
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underwent intra-aneurysmal coil embolization, which resulted in incomplete
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obliteration because the right PCA and the bilateral SCA were incorporated into the
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body of the aneurysm (Figure 6B). Her postoperative course was uneventful,
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although six months later cerebral angiography demonstrated major coil compaction
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and regrowth of the residual sac (Figure 6C). Left P1 segment agenesis was
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identified, and the posterior thalamoperforating artery was seen to originate from the
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right P1 segment of the PCA. Thus we chose a combined approach, including
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isolation of the left SCA and stent-assisted intra-aneurysmal coil embolization
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(Figure 6D). The patient’s postoperative course was complicated by hydrocephalus
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that resolved after placing a ventriculoperitoneal shunt. The patient returned to her
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normal activities with a minor memory deficit (mRS score 1). The 2-year control
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angiography confirmed the complete occlusion of the treated aneurysm and
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satisfactory STA-SCA bypass patency (Figure 6E-6H).
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ACCEPTED MANUSCRIPT Discussion
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We assessed the technical safety and efficacy of endovascular treatments in
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combination with extracranial-intracranial bypass for the treatment of complex
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intracranial aneurysms not amenable to conventional approaches. Further, we
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classified three combined strategies according to the mode of endovascular procedure
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and the bypass surgery purpose (types A-C). Our results suggest that these combined
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procedures can achieve a high rate of complete obliteration (82.9%) with an
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acceptable rate of aneurysm-related morbidity (13.6 %) and mortality (6.8 %).
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Endovascular treatment with bypass surgery to restore cerebral blood flow
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Endovascular procedures combined with bypass surgery have been performed for
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more than a decade to treat complex intracranial aneurysms (Table 5).13-20 The classic
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application of the technique is endovascular parent artery occlusion combined with
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extracranial-intracranial bypass for the treatment of the proximal ICA complex
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aneurysms (type A strategy). The ability to revascularize an intracranial artery creates
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an alternative option for aneurysm management beyond conventional treatments,
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allowing deliberate arterial occlusion to be performed without risk of ischemic
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complications that would occur without bypass.17 Arterial sacrifice enables proximal
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aneurysm occlusion, distal occlusion, trapping, and flow reversal within aneurysms,
19
and any one of these methods often successfully treats the aneurysm. The
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endovascular aneurysm trapping can give an immediate and definitive result by
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completely isolating the aneurysm from the circulation, although some of these
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procedures were performed entirely with microsurgical techniques.10,17
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Flow-diverting stents are new devices designed to treat complex intracranial
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aneurysms. Treating an intracranial aneurysm located at the proximal segment of the
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ICA with flow diverters is effective, with high rates of complete aneurysm
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occlusion.24 However, aneurysm morphology and presentation may affect the 12
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outcome of endovascular treatment with flow diverters. Symptomatic large aneurysms are associated with a high risk of ischemic and hemorrhagic complications.25 Irregular and fusiform aneurysm morphology and branch vessel runoff can potentially
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contribute to the persistent filling of the aneurysm after flow-diverting stent
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placement.26 Investigators have reported that flow-diverting stent surgery for posterior
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circulation aneurysms resulted in a significant number of patients with ischemia due
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to perforator occlusion.12,24 While tools and devices that allow endovascular treatment
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of many complex aneurysms are now available, there is still a subset of aneurysms
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where combined endovascular and microsurgical bypass procedure is recommended.14
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Endovascular treatment with bypass surgery to isolate incorporated vascular
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branches
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In terminal aneurysms or aneurysms incorporating vascular branches, inflow from the
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afferent vessel is a source of hemodynamic stress, with turbulent intra-aneurysmal flow directed to the branches based on their angle of bifurcation.16,27 If the flow to
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such aneurysms is redirected, the intra-aneurysmal circulation can be changed,
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stabilizing the intra-aneurysmal coil mass. These changes can induce increased
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aneurysmal sac thrombosis as observed in patients treated with the type C strategy in
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this study. Previous studies introduced advanced endovascular techniques such as
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double-catheter techniques for protecting vascular branches incorporated into
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intracerebral aneurysms.28 However, these procedures are complicated to perform and
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result in poor coil density because the placement of coil loops near a branch orifice
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should be avoided. The theoretical risks associated with such complicated
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endovascular techniques may be greater than those of endovascular procedures
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performed after the isolation of branches incorporated into the sac. Revascularization
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remains a uniquely surgical contribution to overall aneurysm management, one to
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which current endovascular techniques cannot contribute.29 13
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Complications
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The rate of complications in the present study is comparable to that of other reported
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series of complex intracranial aneurysms and reflects the difficulty in managing these
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lesions.9,16,30-32 Revascularization can reduce the risks of hypoperfusion in the vasculature distal to the arterial occlusion and the branches isolated by endovascular
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procedures. However, ischemic complications in perforator territories might remain
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in spite of the combination with bypass surgery. It should be noted that the bypass
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procedures reported in this study did not guarantee the patency of perforators arising
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close to a treated aneurysm. Planning such an approach relies on a precise understanding of aneurysm anatomy and morphology and the lesion’s relationship to
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important branches and perforators. The preoperative workup should routinely
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include 3-dimensional reconstructed angiographic imaging.14 In this study, we
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preferred to use neck-bridging stents to cover the orifice of perforators arising close to
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the targeted aneurysms to protect their patency. Strict application of antithrombotic
15
therapy throughout the perioperative period could prevent progressive thrombosis and
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further ischemic complications.
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Hemorrhagic complications of the combined procedures were also of concern.
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Antithrombotic therapy, although indispensable to endovascular procedures, could
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lead to more frequent and severe hemorrhagic complications than those associated
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with conventional surgical or endovascular procedures. Meticulous hemostatic
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techniques during the craniotomy and microsurgical procedures should be employed.
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Antiplatelet drugs in a loading dose should be administered immediately before the
23
endovascular procedures. Heparin neutralization with protamine sulfate at the end of
24
the endovascular procedure can prevent a hyper-fibrinolytic state. A computed
25
tomography of the brain performed after each procedure allows the early detection of
26
intracranial hemorrhagic complications. Proximal clip ligation of the recipient arteries 14
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could prevent stagnant bypass flow due to the lack of demand, and prolong the
2
interval between the bypass surgery and endovascular treatment. The prolonged
3
interval enables step-by-step management of antithrombotic therapy.
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Study limitations The limitations of this study include retrospective approach and the small number of
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patients, which precluded a statistical analysis comparing our result with those
7
obtained using alternative approaches. Further studies and larger case series are
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necessary to assess the efficacy and durability of this treatment.
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Conclusions
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Endovascular treatments in combination with extracranial-intracranial bypass surgery
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resulted in durable, and often definitive, protection against hemorrhage and further aneurysmal growth in our series of complex intracranial aneurysms. The mortality
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rate and clinical outcomes were superior to those associated with the natural history
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of these treatment-resistant aneurysms.
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Disclosure
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The authors have no personal financial or institutional interest in any of the drugs,
19
material, or devices described in this article.
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Disclosure of Funding: None.
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Acknowledgments
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We thank Mrs. Azusa Okuwa and Mr. Yoshitaka Sato (Saikou, Inc.,
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www.saikou-i.co.jp) for illustration artwork. We thank Editage (www.editage.jp) for
25
English language editing.
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Gonzalez NR, Duckwiler G, Jahan R, Murayama Y, Vinuela F. Challenges in the endovascular treatment of giant intracranial aneurysms. Neurosurgery.
18
2008;62:1324-1335 7.
Clinical and angiographic outcome after endovascular management of giant
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intracranial aneurysms. Neurosurgery. 2008;63:662-675
21 22
8.
Lawton MT, Spetzler RF. Surgical management of giant intracranial aneurysms: experience with 171 patients. Clin Neurosurg. 1995;42:245-266
23 24
Jahromi BS, Mocco J, Bang JA, Gologorsky Y, Siddiqui AH, Horowitz MB, et al.
AC C
19
EP
17
9.
Sughrue ME, Salner D, Rayz VL, Lawton MT. Giant intracranial aneurysms:
25
evolution of management in a contemporary surgical series. Neurosurgery.
26
2011;69:1261-1271 17
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10. Kivipelto L, Niemela M, Meling T, Lehecka M, Lehto H, Hernesiniemi J. Bypass
2
surgery of complex middle cerebral artery aneurysms: impact of the exact
3
location in the MCA tree. J Neurosurg. 2014;120:398-408
4
11. Wang J, Liu XF, Li BM, Li S, Cao XY, Liang YP, et al. Application of parallel stent placement in the treatment of unruptured vertebrobasilar fusiform
6
aneurysms. J Neurosurg. 2017;126:45-51
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12. Kallmes DF, Hanel R, Lopes D, Boccardi E, Bonafe A, Cekirge S, et al.
8
International retrospective study of the pipeline embolization device: a
9
SC
7
multicenter aneurysm treatment study. AJNR Am J Neuroradiol. 2015;36:108-115 13. Barnett DW, Barrow DL, Joseph GJ. Combined extracranial-intracranial bypass
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and intraoperative balloon occlusion for the treatment of intracavernous and
12
proximal carotid artery aneurysms. Neurosurgery. 1994;35:92-98
13
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14. Choudhri O, Mukerji N, Steinberg GK. Combined endovascular and microsurgical management of complex cerebral aneurysms. Front Neurol.
15
2013;4:108
16
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15. Hacein-Bey L, Connolly ES Jr, Duong H, Vang MC, Lazar RM, Marshall RS, et al. Treatment of inoperable carotid aneurysms with endovascular carotid
18
occlusion after extracranial-intracranial bypass surgery. Neurosurgery.
19
1997;41:1224-1234
21 22 23 24
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20
EP
17
16. Hoh BL, Putman CM, Budzik RF, Carter BS, Ogilvy CH. Combined surgical and endovascular techniques of flow alteration to treat fusiform and complex wide-necked intracranial aneurysms that are unsuitable for clipping or coil
embolization. J Neurosurg. 2001;95:24-35 17. Lawton MT, Quinones-Hinojosa A, Sanai N, Malek JY, Dowd CF. Combined
25
microsurgical and endovascular management of complex intracranial aneurysms.
26
Neurosurgery. 2003;52:263-275 18
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18. Ponce FA, Albuquerque FC, McDougall CG, Han PP, Zabramski JM, Spetzler R.
2
Combined endovascular and microsurgical management of giant and complex
3
unruptured aneurysms. Neurosurg Focus. 2004;17:E11
4
19. Serbinenko FA, Filatov JM, Spallone A, Tchurilov MV, Lazarev VA. Management of giant intracranial ICA aneurysms with combined
6
extracranial-intracranial anastomosis and endovascular occlusion. J Neurosurg.
8 9
1990;73:57-63
20. Shi ZS, Ziegler J, Duckwiler GR, Jahan R, Frazee J, Ausman JI, et al.
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7
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5
Management of giant middle cerebral artery aneurysms with incorporated branches: partial endovascular coiling or combined extracranial-intracranial
11
bypass- a team approach. Neurosurgery. 2009;65:121-131
12
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21. Sato K, Shimizu H, Inoue T, Fujimura M, Matsumoto Y, Kondo R, et al. Angiographic circulation time and cerebral blood flow during balloon test
14
occlusion of the internal carotid artery. J Cereb Blood Flow Metab.
15
2014;34:136-143
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22. Shimizu H, Matsumoto Y, Tominaga T. Parent artery occlusion with bypass
17
surgery for the treatment of internal carotid artery aneurysms: clinical and
18
hemodynamic results. Clin Neurol Neurosurg. 2010;112:32-39 23. Roy D, Milot G, Raymond J. Endovascular treatment of unruptured aneurysms.
22
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19
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16
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2013;44:442-447
20 21
24 25 26
Stroke. 2001;32:1998-2004
24. Brinjikji W, Murad MH, Lanzino G, Cloft HJ, Kallmes DF. Endovascular treatment of intracranial aneurysms with flow diverters: a meta-analysis. Stroke.
25. Becske T, Kallmes DF, Saatci I, McDougall CG, Szikora I, Lanzino G, et al. Pipeline for uncoilable or failed aneurysms: results from multicenter clinical trial. Radiology. 2013;267:858-868 19
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26. Shapiro M, Becske T, Nelson PK. Learning from failure: persistence of
2
aneurysms following pipeline embolization. J Neurosurg. 2017;126:578-585
3
27. Sugiyama S, Niizuma K, Sato K, Rashad S, Kohama M, Endo H, et al. Blood Flow into Basilar Tip Aneurysms: A Predictor for Recanalization After Coil
5
Embolization. Stroke. 2016;47:2541-2547
6
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28. Lubicz B, Lefranc F, Levivier M, Dewitte O, Pirotte B, Brotchi J, et al.
Endovascular treatment of intracranial aneurysms with a branch arising from the
8
sac. AJNR Am J Neuroradiol. 2006;27:142-147
10 11 12 13
29. Cenzato M, Bortolotti C. The role of extra- and intracranial bypass in the treatment of complex aneurysms. J Neurosurg Sci. 2016;60:70-82
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30. Anson JA, Lawton MT, Spetzler RF. Characteristics and surgical treatment of dolichoectatic and fusiform aneurysms. J Neurosurg. 1996;84:185-193 31. Darsaut TE, Darsaut NM, Chang SD, Silverberg GD, Shuer LM, Tian L, et al. Predictors of clinical and angiographic outcome after surgical or endovascular
15
therapy of very large and giant intracranial aneurysms. Neurosurgery.
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2011;68:903-915
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32. Drake CG, Peerless SJ. Giant fusiform intracranial aneurysms: review of 120 patients treated surgically from 1965 to 1992. J Neurosurg. 1997;87:141-162
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ACCEPTED MANUSCRIPT Figure Legends
2
Figure 1. Pre- (A) and postoperative (B) schematic illustrations depicting the
3
combined technique with the type A strategy. When a complex aneurysm involves the
4
parent artery, endovascular occlusion of the parent artery is performed with bypass
5
surgery to restore cerebral blood flow. Simultaneous intra-aneurysmal coil
6
embolization is added in patients with persistent aneurysmal filling via retrograde
7
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flow during the balloon test occlusion of the proximal parent artery.
9
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Figure 2. Pre- (A) and postoperative (B) schematic illustrations depicting the combined technique with the type B strategy. When a complex fusiform aneurysm
11
involves arterial branches, endovascular trapping of the aneurysm is performed with
12
bypass surgery to isolate branches incorporated into the aneurysm.
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Figure 3. Pre- (A) and postoperative (B) schematic illustrations depicting the
15
combined technique with the type C strategy. When a complex saccular aneurysm
16
involves arterial branches, intra-aneurysmal coil embolization with or without a
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neck-bridging stent is performed with bypass surgery to isolate branches incorporated
18
into the aneurysm.
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20
Figure 4. Case 1. (A) Three-dimensional reconstructed angiogram demonstrates a
21
fusiform aneurysm in the supraclinoid segment of the left internal carotid artery
22
(ICA). (B) The left ICA angiogram obtained immediately after endovascular
23
treatment with external carotid artery-middle cerebral artery bypass using a
24
saphenous vein graft shows complete endovascular trapping of the left ICA with coils.
25
(C) Subsequent digital subtraction angiography demonstrates patency of the bypass
26
graft and filling of distal middle cerebral artery branches and the left anterior cerebral 21
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artery. (D) The anterior choroidal artery is visualized via the left posterior
2
communicating artery. (E) Left common carotid artery angiogram obtained after the
3
operation shows satisfactory bypass patency. (F) Schematic illustration depicting the
4
surgical procedure (type A strategy). Asterisks indicated the coil mass.
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Figure 5. Case 2. (A) Preoperative volume-rendered image obtained by magnetic
7
resonance angiography demonstrating the pearl and string feature in the left vertebral artery (VA). The posterior inferior cerebellar artery (PICA) originates from the
9
aneurysmal dilatation of the VA. White arrow indicates the intraluminal hematoma.
SC
8
(B) A radiogram shows the coil mass and clip. (C and D) Digital subtraction
11
angiograms obtained immediately after endovascular trapping of the VA with the
12
occipital artery-PICA bypass demonstrates the disappearance of the VA dissection.
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(E) Left external carotid artery angiogram obtained after the operation shows
14
satisfactory bypass patency. (F) Schematic illustration depicting the surgical
15
procedure (type B strategy). Asterisks indicated the coil mass.
17
Figure 6. Case 3. (A-D) Digital subtraction angiogram showing a large basilar
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bifurcation aneurysm. The right posterior cerebral artery and the bilateral superior
19
cerebellar arteries (SCAs) are incorporated into the sac. (B) Intra-aneurysmal coil
20
embolization allows residual filling of the sac, protecting the patency of the
21
incorporated branches. (C) The residual sac was growing six months after the initial
22
treatment. (D) A combined surgery, including isolation of the left SCA and
23
stent-assisted coil embolization, was performed. (E) Digital subtraction angiogram
24
and (F) radiogram obtained two years after the combined treatment show complete
25
disappearance of the aneurysm. (G) The left external carotid artery angiogram
26
demonstrates patency of the superficial temporal artery-SCA bypass. (H) Schematic
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illustration depicting the surgical procedure (type C strategy).
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Table 1: Baseline Characteristics n
Total
Type A
Type B
Type C
44
12
12
20
Age, y (mean)
29-82 (59.9)
29-82 (60.2) 29-64 (51.0) 39-79 (65.1)
Women
32 (72.7%)
10
6
16
Subarachnoid hemorrhage
24 (54.5%)
6
9
9
Cranial Nerve Palsy
5 (11.4%)
4
0
1
Headache
3 (6.8%)
1
1
1
Brainstem Compression
3 (6.8%)
0
2
1
Hydrocephalus
2 (4.5%)
1
0
1
None
7 (15.9%)
0
Cavernous ICA
5 (11.4%)
5
Supraclinoid ICA
6 (13.6%)
ICA-PcomA
0
7
0
0
6
0
0
2 (4.5%)
0
0
2
MCA
2 (4.5%)
0
0
2
BA bifurcation
5 (11.4%)
1
0
4
BA trunk
1 (2.3%)
0
1
0
BA-SCA
5 (11.4%)
0
0
5
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Symptom
1 (2.3%)
0
1
0
6 (13.6%)
0
0
6
11 (25%)
0
10
1
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Location
AICA VA-PICA VA (V4 segment)
4.4-32.2 (14.1)
Size, mm (mean)
18 (40.9%)
6
1
11
Fusiform
17 (38.6%)
6
11
0
5 (11.4%)
1
1
3
4 (9.1%)
1
1
2
EP
Large/Giant saccular (>12mm)
AC C
Intraluminal thrombus Post-coiling
Abbreviations: ICA, internal carotid artery; PcomA, posterior communicating artery; MCA, middle cerebral artery; BA, basilar artery; SCA, superior cerebellar artery; AICA, anterior inferior cerebellar artery; VA, vertebral artery; PICA, posterior inferior cerebellar artery
1
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Table 2: Treatment Total
Type A
Type B
Type C
Bypass → EVT
40 (90.9%)
12
8
20
EVT → Bypass
4 (9.1%)
0
4
0
Interval
mean 3.2 days
Within 24 hours
32 (72.7%)
12
9
11
Within one week
7 (15.9%)
0
1
More than one week
5 (11.4%)
0
2
Single
33 (75.0%)
5
12
Double
6 (13.6%)
2
Triple
1 (2.3%)
1
High flow (vein graft)
4 (9.1%)
4
3
16
0
4
0
0
0
0
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Anastomosis
6
SC
Bypass Procedure
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Sequence
OA-PICA
18 (34.6%)
0
11
7
STA-MCA
12 (23.1%)
9
0
3
STA-SCA
11 (21.2%)
1
0
10
STA-PCA
6 (11.5%)
2
0
4
4
0
0
1 (1.9%)
0
1
0
24 (49.0%)
12
12
0
25 (51.0%)
5
0
20
15 (34.1%)
0
2
13
8 (18.2%)
1
2
5
OA-AICA Endovascular Procedure Parent artery occlusion Stent use Retreatment
AC C
Complication
EP
Intraaneurysmal coiling
4 (7.7%)
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ECA-MCA (vein graft)
8 (18.2%)
Cerebral infarction
5 (11.4%)
1
2
2
Cerebral contusion
1 (2.3%)
0
0
1
Hemorrhage
2 (4.5%)
1
0
1
Abbreviations: EVT, endovascular treatment; OA, occipital artery; PICA, posterior inferior cerebellar artery; STA, superficial temporal artery; MCA, middle cerebral artery; SCA, superior cerebellar artery; PCA, posterior cerebral artery; ECA, external carotid artery; AICA, anterior inferior cerebellar artery
1
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Table 3: Angiographic Outcome Total
Type A
Type B
Type C
Immediately after surgery (n=44)
n=12
n=12
n=20
Raymond Class 1
29 (65.9%)
11
11
7
2
4 (9.1%)
0
0
4
3
11 (25%)
1
1
9
n=8
n=10
29 (82.9%)
8
9
2
3 (8.6%)
0
0
3
3 (8.6%)
0
1
Raymond Class 1
n=8
Change (n=35) 9 (25.7%)
1
Stable
24 (68.6%)
7
Recanalized
2 (5.7%)
Bypass Good patency
33 (94.3%)
Occlusion
2 (5.7%)
12
3 2
n=10
n=17
0
8
9
8
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Further thrombosis
n=17
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Last follow-up (n=35)
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Aneurysm
0
1
1
n=8
n=10
n=17
7
9
17
1
1
0
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aneurysm
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Raymond Class 1, complete obliteration; Class 2, residual neck; Class 3, residual
1
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Type A
Type B
Type C
0
20 (45.5%)
2
8
10
1
12 (27.3%)
6
1
5
2
2 (4.5%)
1
0
1
3
1 (2.3%)
0
0
1
4
1 (2.3%)
1
0
0
5
3 (6.8%)
0
1
2
6
5 (11.4%)
2
2
1
Morbidity
7 (15.9%)
SC
Table 4: Clinical Outcome
0
1
0
1
0
2
3
2
Cerebral contusion
1
0
2
0
Brainstem compression
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Cerebral infarction
Amyotrophic lateral sclerosis
1
Mortality
5 (11.4%) 1
Aspiration pneumonia
1
Cerebral vasospasm
1
AN rupture
1
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Cardiac failure
1
AC C
EP
Acute subdural hemorrhage
RI PT
Modified Rankin Scale
1
0
1
0
1
0
0
0
1
0
1
0
0
0
1
0
0
0
1
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Table 5: Previous case series with aneurysms treated with endovascular procedures with bypass surgery
Hoh16
1997
2001
Paraclinoid ICA Cavernous ICA
Type A
Complete obliteration
5 6
Type A
1 9
MCA
1
MCA
1
Distal ACA Paraclinoid ICA
1 1
Type A
Type A
Clinical result
RI PT
Angiographic result
N/A
SC
4
Type of treatment
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Hacein-Bey15
1994
Cavernous ICA Paraclinoid ICA Cavernous ICA
Number of patients
Complete
obliteration
Complete obliteration
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Barnett13
1990
Location of aneurysm
EP
Serbinenko19
Year
AC C
Author
N/A Partial obliteration
Complication
None
N/A
None
GR
Occlusion of bypass vessel (1)
GR MD
N/A
GR
N/A
D
Occlusion of bypass vessel (1) Posttreatment aneurysm rupture (1)
Lawton17
2003
N/A
11
N/A
N/A
N/A
Infarction (3)
Ponce18
2004
Cavernous
8
Type A
Complete
GR (14),
Epidural hematoma (5),
1
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2009
PCA Basilar trunk
6
Basilar tip
1
AcomA
1
ACA
1
MCA
MD (3), D (2)
SC
2
6
Occlusion of bypass vessel (1), Infarction (1), Intraoperative aneurysm rupture (1)
Type A
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Shi
20
obliteration
RI PT
ICA
Complete obliteration (5), Near-Complete obliteration (1)
GR (4), Subdural hematoma (1), MD (1), SD Thrombosis (1) (1)
TE D
Abbreviations: ICA, internal carotid artery; MCA, middle cerebral artery; ACA, anterior cerebral artery; PCA, posterior cerebral artery; AcomA,
AC C
EP
anterior communicating artery; GR, good recovery; MD, moderately disabled; SD, severely disabled; D, dead; N/A, not available
2
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ACCEPTED MANUSCRIPT Endovascular treatments in combination with extracranial-intracranial bypass for complex intracranial aneurysms
Highlights
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Some complex aneurysms can be treated with endovascular treatments with bypass.
Endovascular treatments with bypass can be divided into 3 groups.
Surgical morbidity and mortality are acceptable.
SC
Further intraaneurysmal thrombosis can progress after the combined treatments.
AC C
EP
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Prevention of ischemic and hemorrhagic complications is important.
1
S1878-8750(18)30416-9
DOI:
10.1016/j.wneu.2018.02.143
Reference:
WNEU 7558
To appear in:
World Neurosurgery
Received Date: 3 December 2017 Revised Date:
21 February 2018
Accepted Date: 23 February 2018
Please cite this article as: Sato K, Endo H, Fujimura M, Endo T, Matsumoto Y, Shimizu H, Tominaga T, Endovascular treatments in combination with extracranial-intracranial bypass for complex intracranial aneurysms, World Neurosurgery (2018), doi: 10.1016/j.wneu.2018.02.143. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT 1
Endovascular treatments in combination with extracranial-intracranial bypass for complex intracranial aneurysms
2 3
Kenichi Sato, M.D., 1 Hidenori Endo, M.D., 2 Miki Fujimura, M.D., 3 Toshiki Endo,
5
M.D., 3 Yasushi Matsumoto, M.D., 1 Hiroaki Shimizu, M.D., 4 Teiji Tominaga, M.D. 2
RI PT
4
6
9 10 11 12
Department of Neuroendovascular Therapy, Kohnan Hospital, Sendai, Japan
2
Department of Neurosurgery, Tohoku University Graduate School of Medicine,
SC
8
1
Sendai, Japan 3
Department of Neurosurgery, Kohnan Hospital, Sendai, Japan
4
M AN U
7
Department of Neurosurgery, Akita University Graduate School of Medicine, Akita,
Japan
13
Corresponding Author: Kenichi Sato, M.D., Ph.D.
15
Department of Neuroendovascular Therapy, Kohnan Hospital
16
4-20-1, Nagamachi-minami, Taihaku-ku, Sendai, 982-8523, Japan
17
Telephone: 81-22-248-2131
18
Fax: 81-22-248-1966
20
EP
Email: [email protected]
AC C
19
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14
21
Key Words: bypass surgery, cerebral aneurysm, cerebral revascularization,
22
endovascular treatment, fusiform aneurysm, large aneurysm
23
1
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Abbreviations:
3
BTO: balloon test occlusion
4
ECA: external carotid artery
5
ICA: internal carotid artery
6
MCA: middle cerebral artery
7
mRS: modified Rankin Scale
8
OA: occipital artery
9
PCA: posterior cerebral artery
SC
2
RI PT
1
PICA: posterior inferior cerebellar artery
11
SPECT: single-photon emission computed tomography
12
SCA: superior cerebellar artery
13
STA: superficial temporal artery
EP AC C
15
TE D
14
M AN U
10
2
ACCEPTED MANUSCRIPT Abstract
2
Objective: Although most intracranial aneurysms can be treated with microsurgery or
3
endovascular procedure alone, a subset of aneurysms may require a combined
4
approach. The purpose of this study was to assess the efficacy of endovascular
5
interventions combined with bypass surgery for the treatment of complex intracranial
6
aneurysms.
7
Methods: We retrospectively reviewed medical records from a prospectively
8
maintained patient database to identify patients who underwent endovascular
9
treatment of an intracranial aneurysm at our institutes from 2007 to 2017. We
11
SC
recruited patients who received a pre-planned combination of endovascular treatment
M AN U
10
RI PT
1
and extracranial-intracranial bypass surgery.
Results: Forty-four patients (44 aneurysms) were treated with a combined approach.
13
Twenty-four patients presented with subarachnoid hemorrhage. Treatment strategies
14
included endovascular parent artery occlusion with the bypass surgery to restore
15
cerebral blood flow (n=12), endovascular trapping with bypass surgery to isolate
TE D
12
incorporated branches (n=12), and intra-aneurysmal coil embolization with bypass
17
surgery to isolate incorporated branches (n=20). During a mean period of 35.6 months,
18
follow-up catheter angiography was performed in 35 of 44 patients (79.5%) and demonstrated complete aneurysm obliteration in 29 patients (82.9%) and bypass
AC C
19
EP
16
20
patency in 33 (94.3%). The postoperative aneurysm-related mortality and morbidity
21
rates were 6.8% and 13.6%, respectively.
22
Conclusion: Combined endovascular and surgical bypass procedures are useful for
23
the treatment of complex intracranial aneurysms when conventional surgical or
24
endovascular techniques are not feasible and show acceptable rates of morbidity and
25
mortality.
26 27
3
ACCEPTED MANUSCRIPT Introduction
2
Patients with large and giant saccular or fusiform intracranial aneurysms commonly
3
manifest mass effect-related symptoms, ischemic stroke secondary to occlusion of
4
involving perforating branches or thromboembolism, and subarachnoid hemorrhage.1
5
Because the natural history of these aneurysms leads to disastrous clinical outcomes,
6
it is widely agreed that they should not be left untreated.2-5
RI PT
1
The treatment of these complex intracranial aneurysms may be challenging in spite
8
of advances in endovascular procedures and the introduction of refined microsurgical
9
techniques.6-9 Large and giant saccular aneurysms may have wide necks with major
10
branches or perforating arteries incorporated at the neck or the dome, atherosclerotic
11
or calcified walls, and a partially thrombosed lumen. Fusiform aneurysms have no
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SC
7
neck at all, as the entire wall of the involved arterial segment is pathologically
13
dilated, and the lumen may be partially thrombosed. Thus, these lesions are not
14
amenable to conventional surgical treatments.3,10,11 Even the use of advanced
15
endovascular devices such as flow diverters may result in high complication rates and
16
poor angiographic results, especially in posterior circulation aneurysms.12
19
EP
18
When conventional surgical management is not feasible, complex aneurysms can be managed by combining endovascular techniques and microsurgical revascularization, although a limited number of studies describing this combined
AC C
17
TE D
12
20
approach to aneurysm treatment have been published.13-20 In this study, we
21
retrospectively reviewed our experience with combined endovascular treatment and
22
extracranial-intracranial bypass surgery. The purpose of this study was to evaluate the
23
efficacy and technical safety of endovascular procedures combined with bypass
24
surgery in complex aneurysms that were not amenable to conventional approaches.
25 26
Methods 4
ACCEPTED MANUSCRIPT Patients
2
We retrospectively reviewed medical records from a prospectively maintained patient
3
database to identify all patients who underwent endovascular treatment of an
4
intracranial aneurysm at our institutes from May 2007 to June 2017. We recruited
5
those who received a combination of endovascular treatment and
6
extracranial-intracranial bypass surgery. Those whose bypass procedure was not
7
pre-planned, e.g., those who underwent rescue bypass surgery for ischemic
8
complications after endovascular treatment, were excluded. We analyzed each
9
patient’s hospital course and perioperative outcome. Long-term clinical follow-up was
10
attempted for each patient through chart review, patient telephone interview, or both.
11
The institutional review board approved this retrospective study and informed consent
12
was obtained for all patients in written form as well as orally.
13
Surgical management
14
Aneurysm treatment decisions were made on an individual basis in conjunction with
15
our multidisciplinary team. Preoperative surgical planning, including the bypass type
16
and whether to perform vessel occlusion or aneurysm embolization, was based on the
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angiographic findings. Treatment strategies included the following:
18
Type A: endovascular parent artery occlusion with bypass surgery to restore cerebral
19
blood flow (Figure 1)
20
Type B: endovascular trapping with bypass surgery to isolate branches incorporated
21
into the aneurysm (Figure 2)
22
Type C: intra-aneurysmal coil embolization with bypass surgery to isolate branches
23
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incorporated into the aneurysm (Figure 3)
24
The type of bypass surgery (single, double, or high-flow bypass using the
25
saphenous vein) was based on the results of preoperative balloon test occlusion
26
(BTO) using single-photon emission computed tomography (SPECT) or 5
ACCEPTED MANUSCRIPT angiography-based BTO21 when the type A strategy was selected for the treatment of
2
internal carotid artery (ICA) aneurysms.22 Otherwise, we preferred to use a single
3
bypass with the superficial temporal artery (STA) or the occipital artery (OA) as the
4
donor to isolate vascular branches incorporated into the aneurysm (types B and C).
5
All surgical treatments were performed under general anesthesia. Patients with
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unruptured aneurysms were prescribed 100mg aspirin three days before bypass
7
surgery. Bypass patency was assessed intraoperatively using direct blood flow
8
measurement by Doppler ultrasound and indocyanine green video angiography and
9
confirmed by catheter angiography before beginning the endovascular procedure.
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Patients were given antiplatelet agents (300mg clopidogrel and 200mg aspirin)
11
through a nasogastric tube immediately after arterial punctures for endovascular
12
treatment. Postoperatively, dual antiplatelet therapy (75mg/day clopidogrel and
13
100mg/day aspirin) was maintained for six months and then changed to clopidogrel
14
monotherapy (75 mg/day) for an additional six months. The activated coagulation
15
time was monitored from the beginning of the endovascular procedure and
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maintained at a target value between 200 and 250 seconds. A dose of heparin (80
17
IU/kg) was injected intravenously followed by the administration of 16 IU/kg of
18
heparin per hour. Heparin neutralization was routinely achieved by the administering
19
50 mg protamine sulfate at the end of endovascular procedures. A computed
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tomography brain scan was performed immediately after each procedure for early
21
detection of intracranial hemorrhagic complications.
22
Outcomes
23
Angiographic findings were evaluated according to the Raymond classification
24
immediately after treatment and at follow-up.23 Postoperative angiographic follow-up
25
was performed at 6, 12, and 24 months, and as needed. Angiographic recurrence was
26
defined as any worsening of the Raymond classification or enlargement of the 6
ACCEPTED MANUSCRIPT 1
residual aneurysm. Bypass patency was also assessed angiographically. When an
2
angiographic recurrence was considered progressive or large enough to be embolized
3
again, retreatment was planned.
4
Neurological outcomes were assessed using the modified Rankin Scale (mRS) score. Perioperative death and major stroke (mRS>2) were defined as
6
procedure-related mortality and morbidity, respectively. Each patient was evaluated
7
using mRS score at follow-up, and any worsening was recorded.
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Results Patient and Aneurysms Characteristics
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During the study period, 1,683 aneurysms were treated using endovascular techniques.
12
Of these, 44 aneurysms (2.6%) in 44 patients (male, n=12; mean age, 59.9 years; age
13
range, 29-82 years) received endovascular treatment combined with
14
extracranial-intracranial bypass surgery. Clinical presentations included subarachnoid
15
hemorrhage (n=24), cranial nerve palsy (n=5), headache (n=3), brainstem
16
compression (n=3), hydrocephalus (n=2), and no symptoms (n=7). Aneurysms were
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located in the anterior circulation (n=15, 34.1%) and posterior circulation (n=29,
18
65.9%). Twenty-seven aneurysms had saccular morphology, including 18 large or
19
giant aneurysms. Four aneurysms had been previously treated elsewhere with coil
20
embolization with or without stents (Table 1)
21
Surgical Treatment
22
Table 2 summarizes the surgical procedures performed. We used the type A strategy
23
in 12 patients (27.3%), type B in 12 (27.3%), and type C in 20 (45.5%). The bypass
24
procedure was followed by endovascular treatment in 40 patients (90.9%). In four
25
patients with a ruptured vertebral arterial dissection involving the origin of the
26
posterior inferior cerebellar artery (PICA), we performed endovascular proximal
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occlusion in the acute stage, and then trapped the dissected vertebral artery with
2
OA-PICA bypass surgery in the chronic stage. The interval between the bypass
3
surgery and endovascular treatment was within 24 hours in 32 patients (72.7%),
4
within one week in 7 (15.9%), and greater than one week in 5 (11.4%). There were 52 bypass procedures performed in the 44 patients. Three STA-middle
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cerebral artery (MCA) bypasses were a double bypass in which both frontal and
7
parietal branches of the STA were used. A double bypass procedure involving
8
STA-posterior cerebral artery (PCA) and STA-superior cerebellar artery (SCA)
9
bypasses was performed in three patients. Four patients without tolerance to ICA
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occlusion underwent external carotid artery (ECA)-MCA bypass using a saphenous
11
vein graft.
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There were 49 endovascular procedures including parent artery occlusion (n=12), aneurysm trapping (n=12) and intra-aneurysmal coil embolization (n=25). Five
14
patients with ICA aneurysms underwent simultaneous intra-aneurysmal coiling and
15
parent artery occlusion. Stent-assisted intra-aneurysmal coil embolization was
16
performed in 15 patients (34.1%). Eight patients (18.2%) required repeated
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endovascular treatments, including additional coil placement in a recanalized
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aneurysmal sac in five, and parent artery occlusion in three.
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Angiographic Outcomes
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Angiographic results are summarized in Table 3. Angiograms obtained immediately
21
after the procedures revealed complete aneurysm obliteration in 29 patients (65.9%),
22
a residual neck in 4 (9.1%), and a residual aneurysm in 11 (25.0%). Angiographic
23
follow-up at 14.9 ± 3.2 months after the treatment was available in 35 patients
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(79.5%). We achieved complete aneurysm obliteration by parent artery occlusion or
25
trapping with coils in 6 patients (13.6%), thus obviating the need for follow-up
26
catheter angiography. Three patients (6.8%) died within six months of treatments. In 8
ACCEPTED MANUSCRIPT 1
9 of 35 patients (25.7%), follow-up angiograms revealed further thrombosis of the
2
aneurysmal sac. The final results included 29 (82.9%) complete occlusions, 3 (8.6%)
3
residual necks, and 3 (8.6%) residual aneurysms.
4
Follow-up angiograms revealed a satisfactory bypass patency in 33 of 35 patients (94.3%). One patient with a ruptured vertebral artery dissection underwent
6
endovascular trapping of the dissection in combination with right OA-PICA bypass.
7
Diffusion-weighted images performed the following day demonstrated acute
8
infarction in the right cerebellar hemisphere, and magnetic resonance angiography did
9
not show bypass patency. Another patient suffered from severe brainstem infarction
10
due to progressive thrombosis after bilateral vertebral artery coil occlusion with the
11
right STA-PCA and STA-SCA bypasses and isolation of the left PCA for a large
12
symptomatic basilar bifurcation aneurysm. Her right STA-PCA anastomoses, as well
13
as the treated aneurysm, had progressively thrombosed after the left PCA was
14
isolated.
15
Clinical Outcomes
16
Table 4 shows the mRS scores for each treatment strategy. Overall, a good outcome
17
(mRS score of 0-2) was observed in 34 patients (77.3%), and a poor outcome (mRS
18
score of 3-6) was observed in 10 (22.7%). The mean length of postoperative
19
follow-up for all patients was 35.6 ± 4.6 months.
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Five patients (11.4%) died in the follow-up period, including 3 (6.8%) with
21
aneurysm related complications. One patient with an unruptured PICA aneurysm
22
treated with intra-aneurysmal coil embolization combined with OA-PICA bypass died
23
in the postoperative period due to an acute subdural hematoma. One patient with a
24
giant basilar trunk aneurysm died of subarachnoid hemorrhage three months after
25 26
treatment. One patient with a ruptured giant supraclinoid ICA aneurysm treated with parent artery coil occlusion and double STA-MCA bypass died because of severe 9
ACCEPTED MANUSCRIPT 1
cerebral vasospasm. Two patients died of medical complications, including cardiac
2
failure (n=1) and pneumonia (n=1). Seven patients (15.9%) had a lower mRS score in the follow-up period than they
4
had preoperatively, including 6 (13.6%) patients with aneurysm related complications .
5
Of these patients, three (6.8%) had permanent deficits as a result of treatment-related
6
complications including two with a cerebral infarction and one with a cerebral
7
contusion. Two patients with a symptomatic large basilar bifurcation aneurysm
8
underwent endovascular treatment with bypasses, which resulted in residual filling of
9
the aneurysm. These patients presented with a disturbance of consciousness
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postoperatively due to brainstem compression by the treated aneurysm.
11 12
Illustrative Cases
13
Case 1 (type A strategy)
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A 49-year-old woman presented with subarachnoid hemorrhage (WFNS grade
)
15
due to a ruptured fusiform aneurysm at the supraclinoid segment of the left ICA.
16
Cerebral angiography revealed the size of the aneurysm was 6.8 × 6.7 × 5.9 mm
17
and the left ophthalmic artery originated from the dome of the aneurysm (Figure 4A).
18
She underwent SPECT-based BTO, which demonstrated that the left cerebral
19
hemisphere blood flow was 65% lower than the flow on the contralateral side and
20
retrograde filling of the aneurysm via the left ophthalmic artery during the occlusion
21
of the left ICA. High-flow bypass was performed immediately followed by
22
endovascular trapping of the fusiform aneurysm (Figure 4B). Postoperative
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23
angiography showed the complete disappearance of the aneurysm and satisfactory
24
bypass graft patency (Figure 4C – 4F). The patient returned to normal daily activities
25
without any neurological deficits.
26
Case 2 (type B strategy) 10
ACCEPTED MANUSCRIPT A 58-year-old woman experienced the sudden onset of a severe headache without
2
subarachnoid hemorrhage. Magnetic resonance imaging detected a left intracranial
3
vertebral artery dissection (Figure 5A). The left PICA was arising from the
4
aneurysmal dilatation. She was managed conservatively, but the dissecting aneurysm
5
gradually enlarged. We performed endovascular trapping of the dissecting aneurysm
6
with OA-PICA bypass (Figure 5B). The patient’s postoperative course was
7
uneventful. Cerebral angiograms obtained six months after treatment demonstrated
8
complete disappearance of the dissecting aneurysm and satisfactory bypass patency
9
(Figure 5C – 5F).
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Case 3 (type C strategy)
11
A 64-year-old woman presented with subarachnoid hemorrhage (WFNS grade
12
due to a ruptured 17.6-mm-diameter basilar bifurcation aneurysm (Figure 6A). She
13
underwent intra-aneurysmal coil embolization, which resulted in incomplete
14
obliteration because the right PCA and the bilateral SCA were incorporated into the
15
body of the aneurysm (Figure 6B). Her postoperative course was uneventful,
16
although six months later cerebral angiography demonstrated major coil compaction
17
and regrowth of the residual sac (Figure 6C). Left P1 segment agenesis was
18
identified, and the posterior thalamoperforating artery was seen to originate from the
19
right P1 segment of the PCA. Thus we chose a combined approach, including
20
isolation of the left SCA and stent-assisted intra-aneurysmal coil embolization
21
(Figure 6D). The patient’s postoperative course was complicated by hydrocephalus
22
that resolved after placing a ventriculoperitoneal shunt. The patient returned to her
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23
normal activities with a minor memory deficit (mRS score 1). The 2-year control
24
angiography confirmed the complete occlusion of the treated aneurysm and
25
satisfactory STA-SCA bypass patency (Figure 6E-6H).
26
11
)
ACCEPTED MANUSCRIPT Discussion
2
We assessed the technical safety and efficacy of endovascular treatments in
3
combination with extracranial-intracranial bypass for the treatment of complex
4
intracranial aneurysms not amenable to conventional approaches. Further, we
5
classified three combined strategies according to the mode of endovascular procedure
6
and the bypass surgery purpose (types A-C). Our results suggest that these combined
7
procedures can achieve a high rate of complete obliteration (82.9%) with an
8
acceptable rate of aneurysm-related morbidity (13.6 %) and mortality (6.8 %).
9
Endovascular treatment with bypass surgery to restore cerebral blood flow
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Endovascular procedures combined with bypass surgery have been performed for
11
more than a decade to treat complex intracranial aneurysms (Table 5).13-20 The classic
12
application of the technique is endovascular parent artery occlusion combined with
13
extracranial-intracranial bypass for the treatment of the proximal ICA complex
14
aneurysms (type A strategy). The ability to revascularize an intracranial artery creates
15
an alternative option for aneurysm management beyond conventional treatments,
16
allowing deliberate arterial occlusion to be performed without risk of ischemic
17
complications that would occur without bypass.17 Arterial sacrifice enables proximal
18
aneurysm occlusion, distal occlusion, trapping, and flow reversal within aneurysms,
19
and any one of these methods often successfully treats the aneurysm. The
20
endovascular aneurysm trapping can give an immediate and definitive result by
21
completely isolating the aneurysm from the circulation, although some of these
22
procedures were performed entirely with microsurgical techniques.10,17
23
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Flow-diverting stents are new devices designed to treat complex intracranial
24
aneurysms. Treating an intracranial aneurysm located at the proximal segment of the
25
ICA with flow diverters is effective, with high rates of complete aneurysm
26
occlusion.24 However, aneurysm morphology and presentation may affect the 12
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outcome of endovascular treatment with flow diverters. Symptomatic large aneurysms are associated with a high risk of ischemic and hemorrhagic complications.25 Irregular and fusiform aneurysm morphology and branch vessel runoff can potentially
4
contribute to the persistent filling of the aneurysm after flow-diverting stent
5
placement.26 Investigators have reported that flow-diverting stent surgery for posterior
6
circulation aneurysms resulted in a significant number of patients with ischemia due
7
to perforator occlusion.12,24 While tools and devices that allow endovascular treatment
8
of many complex aneurysms are now available, there is still a subset of aneurysms
9
where combined endovascular and microsurgical bypass procedure is recommended.14
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Endovascular treatment with bypass surgery to isolate incorporated vascular
11
branches
12
In terminal aneurysms or aneurysms incorporating vascular branches, inflow from the
13
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afferent vessel is a source of hemodynamic stress, with turbulent intra-aneurysmal flow directed to the branches based on their angle of bifurcation.16,27 If the flow to
15
such aneurysms is redirected, the intra-aneurysmal circulation can be changed,
16
stabilizing the intra-aneurysmal coil mass. These changes can induce increased
17
aneurysmal sac thrombosis as observed in patients treated with the type C strategy in
18
this study. Previous studies introduced advanced endovascular techniques such as
19
double-catheter techniques for protecting vascular branches incorporated into
20
intracerebral aneurysms.28 However, these procedures are complicated to perform and
21
result in poor coil density because the placement of coil loops near a branch orifice
22
should be avoided. The theoretical risks associated with such complicated
23
endovascular techniques may be greater than those of endovascular procedures
24
performed after the isolation of branches incorporated into the sac. Revascularization
25
remains a uniquely surgical contribution to overall aneurysm management, one to
26
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which current endovascular techniques cannot contribute.29 13
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Complications
2
The rate of complications in the present study is comparable to that of other reported
3
series of complex intracranial aneurysms and reflects the difficulty in managing these
4
lesions.9,16,30-32 Revascularization can reduce the risks of hypoperfusion in the vasculature distal to the arterial occlusion and the branches isolated by endovascular
6
procedures. However, ischemic complications in perforator territories might remain
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in spite of the combination with bypass surgery. It should be noted that the bypass
8
procedures reported in this study did not guarantee the patency of perforators arising
9
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7
close to a treated aneurysm. Planning such an approach relies on a precise understanding of aneurysm anatomy and morphology and the lesion’s relationship to
11
important branches and perforators. The preoperative workup should routinely
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include 3-dimensional reconstructed angiographic imaging.14 In this study, we
13
preferred to use neck-bridging stents to cover the orifice of perforators arising close to
14
the targeted aneurysms to protect their patency. Strict application of antithrombotic
15
therapy throughout the perioperative period could prevent progressive thrombosis and
16
further ischemic complications.
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Hemorrhagic complications of the combined procedures were also of concern.
18
Antithrombotic therapy, although indispensable to endovascular procedures, could
19
lead to more frequent and severe hemorrhagic complications than those associated
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20
with conventional surgical or endovascular procedures. Meticulous hemostatic
21
techniques during the craniotomy and microsurgical procedures should be employed.
22
Antiplatelet drugs in a loading dose should be administered immediately before the
23
endovascular procedures. Heparin neutralization with protamine sulfate at the end of
24
the endovascular procedure can prevent a hyper-fibrinolytic state. A computed
25
tomography of the brain performed after each procedure allows the early detection of
26
intracranial hemorrhagic complications. Proximal clip ligation of the recipient arteries 14
ACCEPTED MANUSCRIPT 1
could prevent stagnant bypass flow due to the lack of demand, and prolong the
2
interval between the bypass surgery and endovascular treatment. The prolonged
3
interval enables step-by-step management of antithrombotic therapy.
4
Study limitations The limitations of this study include retrospective approach and the small number of
6
patients, which precluded a statistical analysis comparing our result with those
7
obtained using alternative approaches. Further studies and larger case series are
8
necessary to assess the efficacy and durability of this treatment.
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Conclusions
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Endovascular treatments in combination with extracranial-intracranial bypass surgery
12
resulted in durable, and often definitive, protection against hemorrhage and further aneurysmal growth in our series of complex intracranial aneurysms. The mortality
14
rate and clinical outcomes were superior to those associated with the natural history
15
of these treatment-resistant aneurysms.
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Disclosure
18
The authors have no personal financial or institutional interest in any of the drugs,
19
material, or devices described in this article.
20
Disclosure of Funding: None.
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Acknowledgments
23
We thank Mrs. Azusa Okuwa and Mr. Yoshitaka Sato (Saikou, Inc.,
24
www.saikou-i.co.jp) for illustration artwork. We thank Editage (www.editage.jp) for
25
English language editing.
26
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ACCEPTED MANUSCRIPT Figure Legends
2
Figure 1. Pre- (A) and postoperative (B) schematic illustrations depicting the
3
combined technique with the type A strategy. When a complex aneurysm involves the
4
parent artery, endovascular occlusion of the parent artery is performed with bypass
5
surgery to restore cerebral blood flow. Simultaneous intra-aneurysmal coil
6
embolization is added in patients with persistent aneurysmal filling via retrograde
7
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flow during the balloon test occlusion of the proximal parent artery.
9
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Figure 2. Pre- (A) and postoperative (B) schematic illustrations depicting the combined technique with the type B strategy. When a complex fusiform aneurysm
11
involves arterial branches, endovascular trapping of the aneurysm is performed with
12
bypass surgery to isolate branches incorporated into the aneurysm.
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Figure 3. Pre- (A) and postoperative (B) schematic illustrations depicting the
15
combined technique with the type C strategy. When a complex saccular aneurysm
16
involves arterial branches, intra-aneurysmal coil embolization with or without a
TE D
14
neck-bridging stent is performed with bypass surgery to isolate branches incorporated
18
into the aneurysm.
AC C
19
EP
17
20
Figure 4. Case 1. (A) Three-dimensional reconstructed angiogram demonstrates a
21
fusiform aneurysm in the supraclinoid segment of the left internal carotid artery
22
(ICA). (B) The left ICA angiogram obtained immediately after endovascular
23
treatment with external carotid artery-middle cerebral artery bypass using a
24
saphenous vein graft shows complete endovascular trapping of the left ICA with coils.
25
(C) Subsequent digital subtraction angiography demonstrates patency of the bypass
26
graft and filling of distal middle cerebral artery branches and the left anterior cerebral 21
ACCEPTED MANUSCRIPT 1
artery. (D) The anterior choroidal artery is visualized via the left posterior
2
communicating artery. (E) Left common carotid artery angiogram obtained after the
3
operation shows satisfactory bypass patency. (F) Schematic illustration depicting the
4
surgical procedure (type A strategy). Asterisks indicated the coil mass.
RI PT
5 6
Figure 5. Case 2. (A) Preoperative volume-rendered image obtained by magnetic
7
resonance angiography demonstrating the pearl and string feature in the left vertebral artery (VA). The posterior inferior cerebellar artery (PICA) originates from the
9
aneurysmal dilatation of the VA. White arrow indicates the intraluminal hematoma.
SC
8
(B) A radiogram shows the coil mass and clip. (C and D) Digital subtraction
11
angiograms obtained immediately after endovascular trapping of the VA with the
12
occipital artery-PICA bypass demonstrates the disappearance of the VA dissection.
M AN U
10
(E) Left external carotid artery angiogram obtained after the operation shows
14
satisfactory bypass patency. (F) Schematic illustration depicting the surgical
15
procedure (type B strategy). Asterisks indicated the coil mass.
17
Figure 6. Case 3. (A-D) Digital subtraction angiogram showing a large basilar
EP
16
TE D
13
bifurcation aneurysm. The right posterior cerebral artery and the bilateral superior
19
cerebellar arteries (SCAs) are incorporated into the sac. (B) Intra-aneurysmal coil
20
embolization allows residual filling of the sac, protecting the patency of the
21
incorporated branches. (C) The residual sac was growing six months after the initial
22
treatment. (D) A combined surgery, including isolation of the left SCA and
23
stent-assisted coil embolization, was performed. (E) Digital subtraction angiogram
24
and (F) radiogram obtained two years after the combined treatment show complete
25
disappearance of the aneurysm. (G) The left external carotid artery angiogram
26
demonstrates patency of the superficial temporal artery-SCA bypass. (H) Schematic
AC C
18
22
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illustration depicting the surgical procedure (type C strategy).
AC C
1
23
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Table 1: Baseline Characteristics n
Total
Type A
Type B
Type C
44
12
12
20
Age, y (mean)
29-82 (59.9)
29-82 (60.2) 29-64 (51.0) 39-79 (65.1)
Women
32 (72.7%)
10
6
16
Subarachnoid hemorrhage
24 (54.5%)
6
9
9
Cranial Nerve Palsy
5 (11.4%)
4
0
1
Headache
3 (6.8%)
1
1
1
Brainstem Compression
3 (6.8%)
0
2
1
Hydrocephalus
2 (4.5%)
1
0
1
None
7 (15.9%)
0
Cavernous ICA
5 (11.4%)
5
Supraclinoid ICA
6 (13.6%)
ICA-PcomA
0
7
0
0
6
0
0
2 (4.5%)
0
0
2
MCA
2 (4.5%)
0
0
2
BA bifurcation
5 (11.4%)
1
0
4
BA trunk
1 (2.3%)
0
1
0
BA-SCA
5 (11.4%)
0
0
5
TE D
SC
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Symptom
1 (2.3%)
0
1
0
6 (13.6%)
0
0
6
11 (25%)
0
10
1
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Location
AICA VA-PICA VA (V4 segment)
4.4-32.2 (14.1)
Size, mm (mean)
18 (40.9%)
6
1
11
Fusiform
17 (38.6%)
6
11
0
5 (11.4%)
1
1
3
4 (9.1%)
1
1
2
EP
Large/Giant saccular (>12mm)
AC C
Intraluminal thrombus Post-coiling
Abbreviations: ICA, internal carotid artery; PcomA, posterior communicating artery; MCA, middle cerebral artery; BA, basilar artery; SCA, superior cerebellar artery; AICA, anterior inferior cerebellar artery; VA, vertebral artery; PICA, posterior inferior cerebellar artery
1
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Table 2: Treatment Total
Type A
Type B
Type C
Bypass → EVT
40 (90.9%)
12
8
20
EVT → Bypass
4 (9.1%)
0
4
0
Interval
mean 3.2 days
Within 24 hours
32 (72.7%)
12
9
11
Within one week
7 (15.9%)
0
1
More than one week
5 (11.4%)
0
2
Single
33 (75.0%)
5
12
Double
6 (13.6%)
2
Triple
1 (2.3%)
1
High flow (vein graft)
4 (9.1%)
4
3
16
0
4
0
0
0
0
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Anastomosis
6
SC
Bypass Procedure
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Sequence
OA-PICA
18 (34.6%)
0
11
7
STA-MCA
12 (23.1%)
9
0
3
STA-SCA
11 (21.2%)
1
0
10
STA-PCA
6 (11.5%)
2
0
4
4
0
0
1 (1.9%)
0
1
0
24 (49.0%)
12
12
0
25 (51.0%)
5
0
20
15 (34.1%)
0
2
13
8 (18.2%)
1
2
5
OA-AICA Endovascular Procedure Parent artery occlusion Stent use Retreatment
AC C
Complication
EP
Intraaneurysmal coiling
4 (7.7%)
TE D
ECA-MCA (vein graft)
8 (18.2%)
Cerebral infarction
5 (11.4%)
1
2
2
Cerebral contusion
1 (2.3%)
0
0
1
Hemorrhage
2 (4.5%)
1
0
1
Abbreviations: EVT, endovascular treatment; OA, occipital artery; PICA, posterior inferior cerebellar artery; STA, superficial temporal artery; MCA, middle cerebral artery; SCA, superior cerebellar artery; PCA, posterior cerebral artery; ECA, external carotid artery; AICA, anterior inferior cerebellar artery
1
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Table 3: Angiographic Outcome Total
Type A
Type B
Type C
Immediately after surgery (n=44)
n=12
n=12
n=20
Raymond Class 1
29 (65.9%)
11
11
7
2
4 (9.1%)
0
0
4
3
11 (25%)
1
1
9
n=8
n=10
29 (82.9%)
8
9
2
3 (8.6%)
0
0
3
3 (8.6%)
0
1
Raymond Class 1
n=8
Change (n=35) 9 (25.7%)
1
Stable
24 (68.6%)
7
Recanalized
2 (5.7%)
Bypass Good patency
33 (94.3%)
Occlusion
2 (5.7%)
12
3 2
n=10
n=17
0
8
9
8
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Further thrombosis
n=17
SC
Last follow-up (n=35)
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Aneurysm
0
1
1
n=8
n=10
n=17
7
9
17
1
1
0
AC C
EP
aneurysm
TE D
Raymond Class 1, complete obliteration; Class 2, residual neck; Class 3, residual
1
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Type A
Type B
Type C
0
20 (45.5%)
2
8
10
1
12 (27.3%)
6
1
5
2
2 (4.5%)
1
0
1
3
1 (2.3%)
0
0
1
4
1 (2.3%)
1
0
0
5
3 (6.8%)
0
1
2
6
5 (11.4%)
2
2
1
Morbidity
7 (15.9%)
SC
Table 4: Clinical Outcome
0
1
0
1
0
2
3
2
Cerebral contusion
1
0
2
0
Brainstem compression
M AN U
Cerebral infarction
Amyotrophic lateral sclerosis
1
Mortality
5 (11.4%) 1
Aspiration pneumonia
1
Cerebral vasospasm
1
AN rupture
1
TE D
Cardiac failure
1
AC C
EP
Acute subdural hemorrhage
RI PT
Modified Rankin Scale
1
0
1
0
1
0
0
0
1
0
1
0
0
0
1
0
0
0
1
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Table 5: Previous case series with aneurysms treated with endovascular procedures with bypass surgery
Hoh16
1997
2001
Paraclinoid ICA Cavernous ICA
Type A
Complete obliteration
5 6
Type A
1 9
MCA
1
MCA
1
Distal ACA Paraclinoid ICA
1 1
Type A
Type A
Clinical result
RI PT
Angiographic result
N/A
SC
4
Type of treatment
M AN U
Hacein-Bey15
1994
Cavernous ICA Paraclinoid ICA Cavernous ICA
Number of patients
Complete
obliteration
Complete obliteration
TE D
Barnett13
1990
Location of aneurysm
EP
Serbinenko19
Year
AC C
Author
N/A Partial obliteration
Complication
None
N/A
None
GR
Occlusion of bypass vessel (1)
GR MD
N/A
GR
N/A
D
Occlusion of bypass vessel (1) Posttreatment aneurysm rupture (1)
Lawton17
2003
N/A
11
N/A
N/A
N/A
Infarction (3)
Ponce18
2004
Cavernous
8
Type A
Complete
GR (14),
Epidural hematoma (5),
1
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2009
PCA Basilar trunk
6
Basilar tip
1
AcomA
1
ACA
1
MCA
MD (3), D (2)
SC
2
6
Occlusion of bypass vessel (1), Infarction (1), Intraoperative aneurysm rupture (1)
Type A
M AN U
Shi
20
obliteration
RI PT
ICA
Complete obliteration (5), Near-Complete obliteration (1)
GR (4), Subdural hematoma (1), MD (1), SD Thrombosis (1) (1)
TE D
Abbreviations: ICA, internal carotid artery; MCA, middle cerebral artery; ACA, anterior cerebral artery; PCA, posterior cerebral artery; AcomA,
AC C
EP
anterior communicating artery; GR, good recovery; MD, moderately disabled; SD, severely disabled; D, dead; N/A, not available
2
AC C
EP
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TE D
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TE D
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TE D
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ACCEPTED MANUSCRIPT Endovascular treatments in combination with extracranial-intracranial bypass for complex intracranial aneurysms
Highlights
RI PT
Some complex aneurysms can be treated with endovascular treatments with bypass.
Endovascular treatments with bypass can be divided into 3 groups.
Surgical morbidity and mortality are acceptable.
SC
Further intraaneurysmal thrombosis can progress after the combined treatments.
AC C
EP
TE D
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Prevention of ischemic and hemorrhagic complications is important.
1