Flow diversion after aneurysmal subarachnoid hemorrhage (SAH) is the last treatment option for aneurysm occlusion when other methods of aneurysm treatment cannot be used because of the need for dual antiplatelet therapy. The authors’ general protocol for treatment selection after aneurysmal SAH is provided to share with readers our approach to securing the aneurysm before embarking flow diversion for primary treatment or delayed adjunctive treatment to primary coiling. The authors’ experience with flow diversion after aneurysmal SAH, review of pertinent literature, and the future of flow diversion after aneurysmal SAH are discussed.
Key points
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Flow diversion is not the primary treatment of choice after aneurysmal subarachnoid hemorrhage (SAH) but is a reasonable final option if other, safer options are not available to treat the aneurysm.
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In the setting of acute aneurysm rupture, protection of the aneurysm dome by traditional endovascular or microsurgical means followed by delayed flow diversion is a safer choice than primary flow diversion.
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Our experience and review of the literature show the feasibility of flow diversion in the setting of acute rupture either as primary treatment or in a subacute fashion after dome protection.
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Careful patient selection, selective use of coiling, timing of flow diversion after dome protection, and the timing of heparin and antiplatelet therapy in the periprocedural period improve the safety of flow diversion as a strategy in aneurysmal SAH.
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Shield technology may decrease the duration and/or the need for dual antiplatelet therapy, thereby making flow diversion safer in the setting of aneurysm rupture.
International Subarachnoid Aneurysm Trial established endovascular treatment as the primary treatment of ruptured aneurysms
The International Subarachnoid Aneurysm Trial (ISAT) established endovascular treatment as the primary modality of treatment in patients with aneurysmal subarachnoid hemorrhage (SAH) if there was clear equipoise between both surgical clipping and endovascular coiling. The ISAT investigators randomized 2143 patients to clipping versus coiling and found an absolute risk reduction of approximately 7% in death or dependency at 1 year with coiling. Patients in the endovascular treatment group were more likely to be alive and independent at 10 years than were patients in the neurosurgery group (odds ratio [OR], 1·34; 95% confidence interval [CI], 1·07–1·67). Thirty-three patients had a recurrent SAH more than 1 year after their initial hemorrhage (in 17, the SAH was from rupture of the target aneurysm). Rebleeding was more likely after endovascular coiling (1 in 641 patient years; 0.15%) than after neurosurgical clipping (1 in 2041 patient years; 0.05%), but the risk was small in both groups.
Who gets clipped after the International Subarachnoid Aneurysm Trial?
The presence of subarachnoid blood and brain edema in the acute phase of SAH makes surgical dissection difficult but does not affect the technique of endovascular (endosaccular) coiling. Patients who have been treated preferentially by clipping after the ISAT are those who could not safely undergo endovascular therapies, such as patients with wide-necked or fusiform aneurysms with branch incorporation at the neck or middle cerebral artery (MCA) bifurcation aneurysms, or younger patients with good Hunt and Hess grades (1–3) who would benefit from a theoretically more durable treatment in the long run.
International Subarachnoid Aneurysm Trial established endovascular treatment as the primary treatment of ruptured aneurysms
The International Subarachnoid Aneurysm Trial (ISAT) established endovascular treatment as the primary modality of treatment in patients with aneurysmal subarachnoid hemorrhage (SAH) if there was clear equipoise between both surgical clipping and endovascular coiling. The ISAT investigators randomized 2143 patients to clipping versus coiling and found an absolute risk reduction of approximately 7% in death or dependency at 1 year with coiling. Patients in the endovascular treatment group were more likely to be alive and independent at 10 years than were patients in the neurosurgery group (odds ratio [OR], 1·34; 95% confidence interval [CI], 1·07–1·67). Thirty-three patients had a recurrent SAH more than 1 year after their initial hemorrhage (in 17, the SAH was from rupture of the target aneurysm). Rebleeding was more likely after endovascular coiling (1 in 641 patient years; 0.15%) than after neurosurgical clipping (1 in 2041 patient years; 0.05%), but the risk was small in both groups.
Who gets clipped after the International Subarachnoid Aneurysm Trial?
The presence of subarachnoid blood and brain edema in the acute phase of SAH makes surgical dissection difficult but does not affect the technique of endovascular (endosaccular) coiling. Patients who have been treated preferentially by clipping after the ISAT are those who could not safely undergo endovascular therapies, such as patients with wide-necked or fusiform aneurysms with branch incorporation at the neck or middle cerebral artery (MCA) bifurcation aneurysms, or younger patients with good Hunt and Hess grades (1–3) who would benefit from a theoretically more durable treatment in the long run.
Endovascular devices are developing at a rapid pace to enable treatment of more complex aneurysm morphologies and to decrease recurrence rates
Nevertheless, the permanent aneurysm occlusion rate after simple primary coiling is only 40% to 45%. Endovascular devices are rapidly being developed and enabling the treatment of wide-necked and complex aneurysms with stent assistance, bifurcation devices, and flow diverters. Stent assistance and the use of flow diverters have increased the durability of endovascular treatments. These developments in endovascular devices and techniques are diminishing the argument that younger patients need to be treated by microsurgical means to achieve long-lasting aneurysm occlusion.
Our protocol for aneurysmal subarachnoid hemorrhage
At our center, an external ventricular drain (EVD) is placed in patients with aneurysmal SAH who present with Hunt and Hess grades 3 or higher in the emergency room (open to drain at 20 cm above the tragus) after undergoing a non–contrast-enhanced computed tomography (CT) scan of the head. A CT angiogram of the head and neck is obtained after EVD placement. If the CT angiogram shows an aneurysm, a diagnostic cerebral digital subtraction angiogram is performed and plans are made for possible treatment within 24 hours. Until the aneurysm is treated, the patient is monitored in the neurointensive care unit with strict systolic blood pressure control, maintained under 130 mm Hg. The diagnostic angiogram is performed under conscious sedation if the patient is awake unless the patient is uncooperative.
The right femoral artery is accessed with a micropuncture needle. Using a modified Seldinger technique, a 6-French (F) sheath is placed. After performing an angiographic run of the right femoral artery, a 0.89-mm (0.035-inch) Glidewire (Terumo, Somerset, NJ) and a 5-F angled or Simmons II catheter (Terumo) are advanced as a unit to the aortic arch, and the supra-aortic vessels are engaged. Selective catheterization of both internal carotid arteries (ICAs) and the dominant vertebral artery (VA) is performed to obtain optimal images of the entire cerebral circulation. A three-dimensional (3D) rotational angiogram is obtained, and the images are transferred to an external workstation to better appreciate the morphology of the aneurysm, especially the size of the neck and the involvement of branch vessels in the aneurysm neck. Then, we select orthogonal views for microcatheterization of the aneurysm and attempt primary coiling of the aneurysm with or without balloon assistance. The goal of this treatment is primarily dome protection and obliteration of daughter sacs or focal outpouchings (so-called Murphy’s tits), which are common rupture points in aneurysms. Patients in whom primary dome protection is not feasible (blister, fusiform, dissecting, or very wide-necked aneurysms) are assessed for their candidacy for microsurgical obliteration of the aneurysm. If the aneurysm morphology is complex (eg, blister or fusiform aneurysms) and/or if the patient is not a good candidate for surgical clipping (eg, elderly patients and/or those with poor Hunt and Hess grades), flow diversion or stent assistance is attempted to achieve aneurysm occlusion.
Patients are observed in the neurointensive care unit for 14 days after securing the aneurysm (by open or endovascular means), focusing on vasospasm management, gradual weaning from the EVD, and rehabilitation. If the patient was treated by endovascular methods, we perform a repeat diagnostic angiogram to assess aneurysm occlusion before discharge. If the aneurysm is not completely occluded at this point, we perform definitive therapy, which could include either further primary coiling with or without balloon assistance, stent-assisted/device-assisted coiling, or flow diversion before the patient is discharged.
What is flow diversion?
Flow diversion is the placement of a low-porosity, high-mesh-density device in the parent vessel at the aneurysm neck to decrease flow into the aneurysm and redirect the flow to the distal part of the parent vessel. This method facilitates endothelialization of the flow-diverting device and subsequently excludes the aneurysm from the circulation over time. The Pipeline Embolization Device (PED; Medtronic, Minneapolis, MN) has been used for flow diversion in most of our patients because it is the only flow diverter approved by the Food and Drug Administration in the United States. The PED is a 48-wire, mesh-braided stent made of a radiolucent cobalt-chromium alloy, with every fourth strand made of radiopaque platinum-tungsten. Current flow diverters necessitate 3 months of dual antiplatelet therapy and lifelong aspirin to avoid in-stent thrombosis.
Flow diversion is not the preferred treatment after aneurysmal subarachnoid hemorrhage
Flow diversion after aneurysmal SAH is not preferred as the primary modality of treatment because of the risk associated with dual antiplatelet regimens in the setting of acute rupture. Moreover, the performance of invasive procedures in the preprocedural or periprocedural period, which may include the placement of an EVD, central line, shunt, tracheostomy, and/or percutaneous endoscopic gastrostomy tube, as well as a craniotomy for evacuation of hematoma and decompression, carries additional risk for patients who are receiving dual antiplatelet therapy. In addition, flow diversion does not achieve immediate aneurysm occlusion and does not decrease the chances of immediate rerupture compared with primary coiling or clipping.
Patient selection for flow diversion after aneurysmal subarachnoid hemorrhage
Patients are considered candidates for flow diversion after aneurysmal SAH at our center in the following circumstances: (1) the acute setting, when we cannot achieve dome protection by any other means given the morphology of the aneurysm (ie, dissecting, giant, blister, or fusiform) and if the patient is not a candidate for microsurgical clipping of the aneurysm as determined by a multidisciplinary team; and (2) for definitive therapy before discharge if aneurysm occlusion is not observed on the follow-up angiogram at discharge (in patients treated with primary or balloon-assisted coiling). Most aneurysms that require flow diversion are in the paraclinoid and communicating segments of the ICA or intracranial VA with or without involvement of the vertebrobasilar junction.
Antiplatelet therapy
When flow diversion is chosen as the therapy, any required invasive procedures, including the placement of a central line and an EVD, are performed first. The patient then receives a loading dose of 650 mg of aspirin and 600 mg of clopidogrel and the antiplatelet response is checked with VerifyNow assays (Accriva Diagnostics, San Diego, CA). If the patient is not therapeutic (ie, a nonresponder) on aspirin (reaction units value >550), another loading dose of 650 mg of aspirin is administered. If the patient is not therapeutic on clopidogrel (reaction units value ≥200), a loading dose of 180 mg of Brilinta (AstraZeneca, London, United Kingdom) is administered. We check the reaction units’ value after administering the Brilinta loading dose to make sure the value is less than 200 before proceeding with flow diversion (we previously used prasugrel, but Brilinta is our current drug of choice for clopidogrel nonresponders). After the procedure, the patient is maintained on aspirin (325 mg daily) for life and clopidogrel (75 mg daily) or Brilinta (90 mg daily) for approximately 3 months.
Flow-diversion technique
The procedure is performed under conscious sedation if the patient is cooperative. Either a 6-F Envoy DA XB guiding catheter (Codman Neuro, Raynham, MA) or a biaxial system consisting of a 2.24-mm (088-inch) Neuron Max guide (Penumbra Inc, Alameda, CA) and 115-cm Navien 058 intermediate catheter (Medtronic) used for access. The patient is given heparin to maintain an activated coagulation time of greater than 250 seconds after dome protection (if adjunctive coils are used) or after placement of the first PED (if no coils were used; the use of coils and indications for coiling are discussed later). A 150-cm 0.69-mm (0.027-inch) catheter (eg, Marksman [Medtronic], XT-27 [Stryker Neurovascular, Kalamazoo, MI], or Phenom 27 [Medtronic]) is used for microcatheter access distal to the aneurysm with a Synchro 2 wire (Stryker Neurovascular). After distal microcatheter access has been established, the guide system is advanced coaxially as distal as possible to the petrocavernous region or the V4 segment of the VA to provide excellent support for tracking the PED. At that point, the Synchro 2 wire is removed, and a Pipeline Flex device (Medtronic) is loaded in the microcatheter and advanced until the coil tip of the device is just outside the guiding catheter. The redundancy in the microcatheter is reduced by decreasing the slack in the catheter until the catheter tip can be seen moving and the device is then advanced forward. Once the device is distal to the aneurysm, the Envoy DA XB or Navien catheter is coaxially advanced into the posterior genu/horizontal portion of the cavernous sinus or V4 segment of the VA to assist in delivery of the PED from the microcatheter. The coil tip is unsheathed in a straight segment of the cerebral vasculature (commonly in the M1 segment of the MCA). The entire system is retracted with the coil tip unsheathed so that the Pipeline device is just distal to the distal landing zone. The device is then pushed out from the microcatheter. When a sufficient length of the device is exposed, we wait for 1 or 2 minutes to allow the release and expansion of the distal portion of the device to the size of the vessel lumen. The microcatheter is carefully moved from side to side to assist in the release and opening of the distal end of the device. The device is then carefully delivered from the microcatheter using a push-pull technique, while maintaining wall apposition through the entire length of the device and avoiding kinks around turns in the parent vessel. The last part of the device is typically unsheathed and not pushed out so that the resheathing pad is released from the microcatheter and the device comes free. At this point, the microcatheter is brought back over the deployment mechanism to catch the distal end of the Pipeline device and compact the device. The Envoy DA XB or Navien can also brought up to catch the proximal portion of the device and assist in compacting the device. The entire delivery system with the microcatheter is withdrawn, and final runs are obtained.
Our experience with flow diversion after subarachnoid hemorrhage
Eleven patients with 14 aneurysms underwent flow diversion in the acute setting after presenting with SAH at our center between July 2011 and June 2016 (University at Buffalo Institutional Review Board Project MOD00001046). Some of these patients were included in the series reported by Lin and colleagues and/or Linfante and colleagues. There were 8 women and 3 men, with a mean age of 52 ± 13.7 years. The median time from presentation to treatment was 1 day (range, 0–13 days). Eleven aneurysms were located in the anterior circulation (ICA), whereas 3 were located in the posterior circulation (2 in the VA and 1 in the basilar artery [BA]). The mean greatest dimension of the aneurysm was 5 ± 5.3 mm. The shapes of these aneurysms were saccular in 5, blister in 6, fusiform in 1, and dissecting in 2. Two aneurysms had been coiled previously for dome protection. Flow diversion alone was performed for treatment in all cases, except case 11, for which coils were used to support the PED spanning the patient’s fusiform aneurysm. Only 1 PED was deployed in each case. The mean length of procedure was 64 ± 34.5 minutes. A summary of the cases is provided in Table 1 .
| Case Number | Sex | Age (y) | Hunt and Hess Grade | Time from SAH Presentation to PED (d) | Aneurysm Location | Side | Aneurysms (N) | Morphology/Shape | Previous Treatment and Type | Procedure | PEDs (N) | Preoperative Antiplatelet Therapy |
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| 1 | F | 63 | 4 | 1 | ICA: supraclinoid | R | 1 | Blister | None | PED alone | 1 | None |
| 2 | M | 76 | 4 | 13 a | Basilar | NA | 1 | Dissecting | None | PED alone | 1 | Aspirin + Brilinta |
| 3 | F | 57 | 2 | 1 | VA: V4 | L | 1 | Dissecting | None | PED alone | 1 | Aspirin + clopidogrel |
| 4 | M | 54 | 1 | 4 b | ICA: paraophthalmic | L | 1 | Saccular | None | PED alone | 1 | Aspirin + clopidogrel |
| 5 | M | 49 | 2 | 1 | ICA: SHA | R | 1 | Saccular | None | PED alone | 1 | None |
| 6 | F | 49 | 5 | 0 | VA: V4 | R | 1 | Blister | None | PED alone | 1 | Aspirin + clopidogrel |
| 7 | F | 19 | 1 | 0 | ICA: paraophthalmic ICA: clinoid | L | 2 | Blister; blister | None | PED alone | 1 | None |
| 8 | F | 50 | 3 | 7 | ICA: supraclinoid | L | 1 | Saccular | Yes (coiling) | PED alone | 1 | Aspirin + clopidogrel |
| 9 | F | 54 | 5 | 0 | ICA: paraophthalmic ICA: anterior choroidal PComA | L | 3 | Saccular; Blister; Saccular | Yes (Coiling); None; None | PED alone c | 1 | Aspirin + prasugrel |
| 10 | F | 48 | 1 | 0 | ICA: posterior wall | L | 1 | Blister | None | PED alone | 1 | Aspirin + prasugrel |
| 11 | F | 55 | 3 | 0 | ICA: paraclinoid | L | 1 | Fusiform | None | PED and coils | 1 | Aspirin + prasugrel |
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