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Abstract
Flow-diverting devices offer an exciting alternative for the management of large and giant intracranial aneurysms. However, the risk and mechanism of delayed aneurysmal rupture and hemorrhage following placement of these devices are not clearly understood. Two patients with similar symptomatic giant paraclinoid internal carotid artery aneurysms are described. Both patients were treated with SILK flow-diverting devices. In both patients the SILK device was placed without technical complication. The first patient continued to do well 1 year postoperatively with complete aneurysm occlusion. The second patient had a delayed subarachnoid hemorrhage despite markedly decreased filling of the aneurysm immediately following the procedure. Flow-diverting devices are an exciting technology which provide an alternative treatment modality in the management of giant intracranial aneurysms. However, caution must be exercised as the risks of delayed complications have yet to be fully elucidated. Similar aneurysms may have drastically different outcomes due to the unpredictability of this technology.
- Flow diverter
- stent
- aneurysm
- hemorrhage
- blood flow
- atherosclerosis
- angioplasty
- angiography
- artery
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Introduction
The currently available flow-diverting devices are self-expandable high-coverage mesh devices that take advantage of hemodynamics to induce thrombosis in an aneurysm sac, thereby occluding an aneurysm without the need for coiling. Both the Pipeline device (eV3, Plymouth, Minnesota, USA)1–3 and the SILK device (Balt, Montmorency, France)4–7 have been shown to be efficacious and durable in preliminary evaluations. However, despite these promising results, one of the troubling concerns with flow diverters is the risk of delayed hemorrhage.8
We present two patients with similar aneurysms that were treated with the SILK device to highlight two very different outcomes and underscore the uncertainties that remain in using flow diverters.
Case reports
Patient 1
A 53-year-old right-handed patient with a history of hypertension presented with a 1-year history of right eye bulging and 2 months of progressive ptosis and diplopia. Physical examination revealed right-sided pupillary dilation and ptosis. Ophthalmologic examination revealed restricted right eye movement of 90% on elevation and depression, 60% on abduction and 70% on adduction. Movement of the left eye was normal. Visual acuity was preserved. Imaging studies demonstrated a 30 mm right paraclinoid internal carotid artery aneurysm (figure 1A,B). A SILK device was subsequently placed across the diseased segment of the parent vessel without complication. Immediately after treatment the aneurysm demonstrated markedly reduced filling, and complete obliteration was evident 2 weeks postoperatively (figure 1C). At 1-year follow-up the patient continued to have complete aneurysm occlusion without complications (figure 1D).
(A) Axial CT angiogram showing a 30 mm paraclinoid right internal carotid artery aneurysm. (B) The aneurysm on angiogram (right internal carotid injection; anteroposterior view). (C) Angiographic results 21 days following placement of the SILK device showing complete obliteration of the aneurysm (right internal carotid injection; anteroposterior view). (D) Angiogram at 1-year follow-up showing stable aneurysm occlusion (right internal carotid injection; anteroposterior view).
Patient 2
A 48-year-old right-handed patient with a history of hypertension presented with a 2-day history of nausea and vomiting. The neurological examination was unremarkable. Imaging studies revealed a 19 mm left paraclinoid internal carotid artery aneurysm (figure 2A,B). Although the patient passed balloon test occlusion, in view of the patient's age a decision was made to preserve the carotid artery. Two SILK devices were placed in a telescoped overlapping fashion across the aneurysmal portion of the parent artery. Excellent immediate angiographic results were obtained with minimal residual neck filling (figure 2C). The patient was anticoagulated with heparin for 48 h postoperatively and then started on aspirin and clopidogrel. The patient was discharged home on postoperative day 3. One week later the patient was found unresponsive by family members. A CT scan of the head revealed extensive subarachnoid hemorrhage and a subsequent angiogram demonstrated partial recanalization of the aneurysm neck (figure 2D). The patient died 5 days later.
(A) Sagittal CT angiogram showing a 19 mm paraclinoid left internal carotid artery aneurysm. (B) The aneurysm on angiogram (left internal carotid injection; anteroposterior view). (C) Angiographic results immediately following placement of the SILK device (left internal carotid injection; anteroposterior view). (D) Repeat angiogram on postoperative day 10 in the setting of extensive subarachnoid hemorrhage showing recanalization at the level of the aneurysm neck (left internal carotid injection; anteroposterior view).
Discussion
A few relatively small studies have shown the SILK flow diverter to be safe, efficacious and durable within a limited follow-up period.5–7 Death rates for the device of 4–8% and morbidity rates of 5–15% have been reported.5–7 The complete aneurysm occlusion rates observed in these studies were 50–69% at follow-up at 3–6 months.5–7 One study of 26 aneurysms reported an 86% occlusion rate at 1 year.7 The reported results from recent Pipeline studies have suggested death rates between 0% and 2% and morbidity rates between 0% and 4%.1–3 Aneurysm occlusion rates were reported to be 93% at 6 months and 95% at 1 year.1 ,2 By comparison, endovascular coiling has been established as a safe treatment option for many aneurysms, but the outcomes are much worse in the setting of large aneurysms. One series of 39 giant aneurysms treated with endovascular coiling (with or without stent assistance) reported 32% morbidity and 16% mortality rates.9
Larger trials of flow-diverting devices with longer follow-up are required to evaluate the long-term outcomes of these devices. A recent study reported a high rate of delayed hemorrhage following placement of Pipeline flow diverters.8 The authors observed that flow diverter placement can increase the pressure within the aneurysm sac predisposing to rupture, especially in giant aneurysms. This complication has likewise been reported secondary to SILK device placement.10 While the precise risk factors for delayed hemorrhage remain unclear, there is evidence that large aneurysm size, symptomatic aneurysms, aneurysms with a high aspect ratio (>1.6 height:neck width) and particular aneurysm geometry may all predispose to hemorrhage after flow diversion.11 These reports, in addition to the cases presented here, highlight the need for a better understanding of the physiologic events that occur following the placement of a flow diverter in order to minimize both acute and delayed complications.
Flow-diverting devices stagnate blood flow within aneurysms to promote platelet adhesion and ultimately thrombus formation within the aneurysm while leaving the parent artery patent. The formation and stabilization of endosaccular thrombus effectively excludes the aneurysm from the circulation and exposure to pulsatile systemic blood pressure. Over time, the thrombus is resorbed and neointimal remodeling and endothelial proliferation reconstitute the wall of the parent vessel. Critically, this process preserves side branches and perforators from the affected vessel segment.
Accordingly, a major challenge in the management of patients receiving flow diverters is promoting stability of the clot formed to prevent recanalization of the aneurysm without inducing pathologic thrombosis or predisposing to aneurysmal bleeding. The approach relies on a delicate balance between blood stagnation and thrombus formation within an aneurysm, on the one hand, and necessary systemic antiplatelet therapy on the other.
Another emerging factor in the success of flow diverter therapy is the composition of the thrombus formed within the aneurysm. ‘White’ thrombi consist primarily of platelet aggregates with a high percentage of fibrin, while ‘red’ thrombi contain more erythrocytes and leucocytes with a lesser degree of fibrin. Consequently, red thrombi—which form under conditions of stasis such as those initially created within an aneurysm by a flow diverter—are more susceptible to fibrinolytic enzymes.12 One report that documented the fatal subarachnoid hemorrhage of a patient following flow diverter placement found persistence of a red thrombus within the patient's aneurysm.10 The authors postulate that the failure of the initial red thrombus to organize into a white thrombus resulted in the fatal bleed. It has been suggested that large aneurysm size, rapid thrombosis and persistent endosaccular blood flow after flow diversion may predispose to persistent red thrombi.11 Fibrinolytic enzymes released by leucocytes within the red thrombus may ultimately destabilize a clot and lead to aneurysm rupture. This promotes the theory that inflammatory processes within the region of a deployed flow-diverting device contribute to delayed hemorrhage by altering clot and vessel wall stability.
The radiographic results obtained for patient 1 illustrate the physiologic processes at work following placement of a flow-diverting device. In this patient, endosaccular thrombus formation was noted as early as 3 days post-intervention (figure 3A). Likewise, inflammatory changes became evident in the aneurysm postoperatively (figure 3B). It is likely that the combination of these two processes—thrombosis and inflammation—following placement of a flow diverter influences whether delayed hemorrhage occurs. While this patient had a good outcome despite the inflammatory process within the aneurysm, the radiographic studies suggest that inflammation is involved in the healing process following flow diverter placement. The exact role of this inflammation needs to be elucidated.
(A) Axial T2-weighted MRI on postoperative day 3 showing endosaccular thrombus formation in the aneurysm. (B) Axial T1-weighted MRI without contrast on postoperative day 14 showing signal enhancement of the aneurysm margin suggestive of an inflammatory process.
This report illustrates different outcomes in two patients with very similar large aneurysms treated with flow diverters. While the two cases presented here are not identical—one was a giant aneurysm with a subacute presentation treated with a single device while the other was a large aneurysm with a more acute presentation treated with two telescoped devices—they illustrate similar clinical scenarios in which flow diverters may be used. As we continue to collect more information from patients undergoing placement of flow diverters, a critical goal will be to identify those patients who are at the highest risk of delayed subarachnoid hemorrhage. Although flow diverters have provided an exciting additional tool to treat these difficult aneurysms, their unpredictability, though rare, is concerning.
References
Footnotes
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GAK and TW contributed equally to this article.
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Competing interests None.
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Ethics approval Ethics approval was not required as this brief retrospective case report does not pose any risks to the patients described and does not compromise their confidentiality. The cases have been fully anonymized by removing all references to gender.
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Provenance and peer review Not commissioned; externally peer reviewed.