Endovascular treatment of fusiform cerebral aneurysms with the Pipeline Embolization Device

Clinical article

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Object

Despite advances in surgical and endovascular techniques, fusiform aneurysms remain a therapeutic challenge. Introduction of flow-diverting stents has revolutionized the treatment of aneurysms with wide necks and of complex morphology. The authors report their experience with the endovascular treatment of fusiform aneurysms using the Pipeline Embolization Device.

Methods

A retrospective review of 146 patients with cerebral aneurysms treated with the Pipeline Embolization Device between June 2011 and January 2013 was performed. Twenty-four patients were identified as having fusiform aneurysms. Twenty-four aneurysms in these 24 patients were treated. The mean patient age was 59 years. There were 9 men and 15 women. Angiographic and clinical data (including the modified Rankin Scale [mRS] score) were recorded at the time of treatment and at follow-up. The aneurysms were located in the internal carotid artery in 8 patients (33.3%), middle cerebral artery in 8 patients (33.3%), anterior cerebral artery in 1 patient (4%), and vertebrobasilar circulation in 7 patients (29%). The aneurysms were smaller than 10 mm in 3 patients, 10–25 mm in 16 patients, and larger than 25 mm in 5 patients. The mean largest dimension diameter was 18 mm.

Results

Stent deployment was successful in all cases. The minor procedural morbidity was 4% (1 case). Morbidity and mortality related to aneurysm treatment were 4.2% and 4.2%, respectively. The mean mRS scores preoperatively and at clinical follow-up (median 6.0 months, mean 6.9 months) were 0.71 and 1.2, respectively (91.7% presented with an mRS score of 2 or better, and 79.2% had an mRS score of 2 or better at the 6.0-month follow-up). At clinical follow-up, 82.6% of patients were stable or had improved, 13.0% worsened, and 4.2% had died. Twenty-two (91.7%) of 24 patients had follow-up angiography available (mean follow-up time 6.3 months); 59% had excellent angiographic results (> 95% or complete occlusion), 31.8% had complete aneurysm occlusion, 27.3% had greater than 95% aneurysm occlusion, 18.2% had a moderate decrease in size (50%–95%), 4.5% had a minimal decrease in size (< 50%), 13.6% had not changed, and 4.5% had an increase in size.

Conclusions

This series demonstrates that endovascular treatment of fusiform cerebral aneurysms with flow diversion was a safe and effective treatment. Procedural complications were low. Long-term morbidity and mortality rates were acceptable given the complex nature of these lesions.

Abbreviations used in this paper:DSA = digital subtraction angiography; ICA = internal carotid artery; MCA = middle cerebral artery; MRA = MR angiography; mRS = modified Rankin Scale; PED = Pipeline Embolization Device; PICA = posterior inferior cerebellar artery; TIA = transient ischemic attack.

Abstract

Object

Despite advances in surgical and endovascular techniques, fusiform aneurysms remain a therapeutic challenge. Introduction of flow-diverting stents has revolutionized the treatment of aneurysms with wide necks and of complex morphology. The authors report their experience with the endovascular treatment of fusiform aneurysms using the Pipeline Embolization Device.

Methods

A retrospective review of 146 patients with cerebral aneurysms treated with the Pipeline Embolization Device between June 2011 and January 2013 was performed. Twenty-four patients were identified as having fusiform aneurysms. Twenty-four aneurysms in these 24 patients were treated. The mean patient age was 59 years. There were 9 men and 15 women. Angiographic and clinical data (including the modified Rankin Scale [mRS] score) were recorded at the time of treatment and at follow-up. The aneurysms were located in the internal carotid artery in 8 patients (33.3%), middle cerebral artery in 8 patients (33.3%), anterior cerebral artery in 1 patient (4%), and vertebrobasilar circulation in 7 patients (29%). The aneurysms were smaller than 10 mm in 3 patients, 10–25 mm in 16 patients, and larger than 25 mm in 5 patients. The mean largest dimension diameter was 18 mm.

Results

Stent deployment was successful in all cases. The minor procedural morbidity was 4% (1 case). Morbidity and mortality related to aneurysm treatment were 4.2% and 4.2%, respectively. The mean mRS scores preoperatively and at clinical follow-up (median 6.0 months, mean 6.9 months) were 0.71 and 1.2, respectively (91.7% presented with an mRS score of 2 or better, and 79.2% had an mRS score of 2 or better at the 6.0-month follow-up). At clinical follow-up, 82.6% of patients were stable or had improved, 13.0% worsened, and 4.2% had died. Twenty-two (91.7%) of 24 patients had follow-up angiography available (mean follow-up time 6.3 months); 59% had excellent angiographic results (> 95% or complete occlusion), 31.8% had complete aneurysm occlusion, 27.3% had greater than 95% aneurysm occlusion, 18.2% had a moderate decrease in size (50%–95%), 4.5% had a minimal decrease in size (< 50%), 13.6% had not changed, and 4.5% had an increase in size.

Conclusions

This series demonstrates that endovascular treatment of fusiform cerebral aneurysms with flow diversion was a safe and effective treatment. Procedural complications were low. Long-term morbidity and mortality rates were acceptable given the complex nature of these lesions.

Despite advances in surgical techniques and endovascular innovations, fusiform aneurysms remain a formidable challenge for neurosurgeons. They may present with ischemic complications associated with distal embolization, subarachnoid hemorrhage, or neurological deficit from the mass effect and compression of critical neuroanatomical structures.1 These challenges are even more difficult in large or giant fusiform aneurysms. The pioneering work by Drake set the platform of understanding of flow dynamics in these lesions and set about forming the basis of many modern treatment strategies.5 Indeed, hunterian ligation is still used successfully in the treatment of many giant fusiform aneurysms.5,6 Advances in surgical technique saw modest improvements in outcomes; however, the relative rarity and the frequent necessity for complex surgical reconstruction continue to test even the most experienced neurovascular surgeons. The advent of endovascular therapy and the more recent development of flow-diverting stents offered a promising method of treatment. Early experience with flow diverters with large and wide-necked aneurysms was positive.12,13 The current literature on the use of flow diversion for the treatment of fusiform aneurysms is limited to small case series or subgroup analysis from large series. We set out to detail our experience at a single center using the Pipeline Embolization Device (PED; Covidien/ev3) for the treatment of fusiform aneurysms in a high-volume center.

Methods

A retrospective review of 146 patients treated at our institution with the PED (Covidien/ev3) between June 2011 and January 2013 was performed. Angiograms and procedure notes of the 146 cases were reviewed, and 24 patients were found to have fusiform aneurysms that were treated primarily with the PED. Patients who had undergone prior treatment (either surgical or endovascular) were included. Treatments that included coiling in addition to the placement of the PED(s) were also included. Aneurysms were categorized as fusiform based on 3D rotational digital subtraction angiography (DSA) findings, as well as cross-sectional imaging using 3D CT angiography and MR angiography (MRA). Cases were considered for inclusion when the entire diseased vessel segment was dilated without a discrete aneurysm neck. All cases were reviewed for inclusion by the senior author (P.J.). Aneurysms that had a discrete neck or were large “side-walled” aneurysms were excluded. Clinical data, including the modified Rankin Scale (mRS) score, were collected prior to treatment, at discharge, and at follow-up. Angiographic data were collected at the time of the procedure and at 6–12 months. If angiographic data were unavailable or the patient refused follow-up angiography then aneurysm status was evaluated using MRA (time of flight and Gd-enhanced MRI) when available. Aneurysm size (in 3 dimensions) and location were recorded, and the change in size was noted using follow-up angiography. The presence of new contrast stasis after PED placement was noted. Details of the PED (diameter, length, and number of devices) and the recipient vessels (inflow artery diameter and outflow artery diameter) were measured. The length of normal proximal and distal vessel purchase (distance of disease-free vessel covered by the PED before the PED entered the aneurysm) was determined. Perforator coverage (and the number of devices covering them) was examined both during the procedure and at follow-up angiography. Procedural data, including platelet inhibition percentage at the time of procedure and procedural complications, were noted.

Results

Patient Characteristics

Twenty-four aneurysms were treated in 24 patients (Table 1). All aneurysms were unruptured. The mean age was 59 years (range 26–81 years). There were 9 men and 15 women. Seven patients were treated after routine follow-up following prior treatment (5 endovascularly and 2 surgically) revealed residual or recurrent aneurysm. Four patients presented with cranial neuropathy or new neurological deficit due to compressive effects. Two patients presented primarily with severe headache (not subarachnoid hemorrhage). Four patients presented with transient ischemic attack (TIA) or stroke. Six patients had their aneurysm discovered as an incidental finding, and 1 patient had the aneurysm discovered after screening was performed because of a family history of aneurysms. The average mRS score on admission was 0.71 and it was 1.2 at the last follow-up (mean clinical follow-up duration 6.9 months, median 6 months). At presentation 22 (91.7%) of 24 patients had an mRS score of 2 or better; the remaining 2 patients (8.3%) had an mRS score of 3 or higher. At follow-up 19 (79.2%) of 24 patients had an mRS score of 2 or better, and 5 (20.8%) had an mRS score of 3 or greater. One patient who died of metastatic pancreatic cancer after an uncomplicated procedure was excluded from the clinical outcome analysis. Comparing mRS score on admission to last follow-up (Table 2) demonstrated that 2 patients improved (8.7%), 17 remained stable (73.9%), 3 worsened (13.0%), and 1 died (4.3%).

TABLE 1:

Patient characteristics

CharacteristicValue*
sex
 male9 (37.5)
 female15 (62.5)
age in yrs
 mean59
 range26–81
presentation
 follow-up after prior treatment7 (29.2)
 cranial neuropathy4 (16.7)
 headache2 (8.3)
 TIA or stroke4 (16.7)
 incidental6 (25.0)
 screening1 (4.1)

Values are the number of patients (%) unless noted otherwise.

TABLE 2:

Clinical follow-up*

Status at Follow-UpNo. of Patients (%)
improved2 (8.7)
stable17 (73.9)
worse3 (13.0)
death1 (4.3)

The patient who died of cancer was excluded from this analysis.

Based on the mRS scores.

Aneurysm Characteristics

The details of the aneurysms treated are listed in Table 3. The aneurysm was located in the internal carotid artery (ICA) in 8 patients (33.3%), middle cerebral artery (MCA) in 8 patients (33.3%), anterior cerebral artery in 1 patient (4.2%), and vertebrobasilar circulation in 7 patients (29.2%). Aneurysm size was < 10 mm in 3 patients, 10–25 mm in 16 patients, and > 25 mm in 5 patients (0 to <10 mm in 3 patients, 10 to <20 mm in 10 patients, 20 to 30 mm in 10 patients, and > 30 mm in 1 patient). The mean largest diameter was 18.0 mm.

TABLE 3:

Aneurysm characteristics

ParameterNo. of Patients (%)
rupture status
 unruptured24 (100)
 ruptured0 (0)
location
 ICA8 (33.3)
 MCA8 (33.3)
 anterior cerebral artery1 (4.2)
 vertebrobasilar7 (29.2)
size (mm)
 <103 (12.5)
 10–2516 (66.7)
 >255 (20.8)

Procedure

Details of the cases are shown in Table 4. Patients were instructed to take aspirin (81 mg/day) and clopidogrel (75 mg/day) for 10 days prior to treatment. Clopidogrel response with the Accumetrics test was performed prior to the procedure with a goal of 30%–80% inhibition. Analysis of available data in our series demonstrated a mean percentage inhibition of 61% (range 24%–98%). Two patients did not respond to clopidogrel and were placed on a regimen of prasugrel preoperatively. Steroids were not prescribed routinely unless patients developed new symptoms thought to be due to swelling or aneurysm thrombosis postoperatively. Such patients were placed on a regimen of 1-week dexamethasone taper on discharge. Clopidogrel was generally discontinued at 6 months if the aneurysm was completely obliterated on follow-up angiography. Aspirin (81 mg) was continued indefinitely. All patients received heparin for the procedure with an activated clotting time maintained at 2–2.5 times baseline.

TABLE 4:

Case details*

Case No.Age (yrs), SexAN LocationAN Size (mm)Size of Device(s) Used (mm)No. of DevicesNo. of TxPerforator Covered by PEDNo. of PEDs Covering PerforatorsClinical PresentationFU Angiogram Time (mos)FU Angiographic ResultmRS Score on AdmissionmRS Score at FUClinical FU Duration (mos)
181, Fcavernous21 × 29 × 194.75 × 20, 5 × 20 then 5 × 18, 5 × 184 (2 per Tx)2nononediplopia1 wkstasis but not complete occl141
266, MM28 × 7 × 42.5 × 18, 2.5 × 1421yes1–2TIA4complete AN occl006
374, FV411 × 7 × 74 × 14, 3.75 × 2021PICA2recurrence on FU imaging6complete occl of AN; PICA still fills0012
460, MV410 × 10 × 63.75 × 18, 4 × 14, 4 × 1631PICA (large)3incidental finding12minimal filling of AN0013
579, Fcavernous20 × 11 × 194.25 × 2511OphA1severe HA670% ↓ in size, w/ stasis106
661, Fcavernous15 × 10 × 123.25 × 2011OphA1severe HANANA111
750, Fbasilar trunk28 × 11 × 143.5 × 3011AICA1recurrence on FU imaging1450% ↓ in size0014
874, Fcavernous22 × 20 × 195 × 2011nonone↑ AN size on imaging795% AN oblit0010
931, MM114 × 9 × 152.5 × 18, 2.5 × 1621M1 perforators1residual AN post-clipping1295% AN oblit0012
1075, Fcavernous20 × 15 × 193.75 × 18, 3.75 × 16, 3.75 × 1431OphA, AChA2diplopia & severe HA695% AN oblit, tiny endoleak w/ tiny residual1112
1166, Fpetrous12 × 7 × 74.5 × 20, 4.5 × 2021nononeincidental finding6contrast stasis but no change in AN006
1243, Fbasilar trunk9 × 14 × 93.5 × 2011AICA1TIA & HA10complete occl of AN0010
1367, MM117 × 14 × 72.75 × 20, 2.75 × 1621M1 perforators2stroke650% ↓ in size w/ remodeling116
1477, Mbasilar trunk22 × 23 × 205 × 30 (lt VA to rt VA)11basilar perforators1ataxia, 6th nerve palsyNANA267
1573, Fcavernous17 × 18 × 243.5 × 2011OphA1diplopia6complete occl of AN; OphA no longer fills by ICA106
1666, MM125 × 6 × 93.5 × 35, 3.5 × 20, 3.5× 1831M1 perforators1–2MRI for pancreatic cancer workup; TIAsNANA362
1758, Fcarotid cave11 × 4 × 84.25 × 1811OphA1incidental finding650% ↓ in size006
1848, Fpericallosal4 × 5 × 42.5 × 1411callosomarginal1found on imaging posttrauma6complete occl of AN006
1932, Mbasilar trunk38 × 46 × 293.25 × 20, 3.25 × 20, 3.25 × 18, 3.25 × 16 then 3.75 × 18, 3.25 × 206 (4 in 1st, 2 in 2nd Tx)2AICA1multi cranial neuropathies; after multi stent & coiling procedures at outside institution2nd procedure 5 mos post 1st procedureongoing filling of AN prompting addition of 2 PEDs458 (after 1st procedure)
2051, MM112 × 14 × 123.0 × 1611M1 perforators1incidental finding4complete M1 occl; AN obliterated145
2126, FM35 × 5 × 52.5 × 1211M3 branches1screening MRA for family Hx of ANs6complete occl of AN006
2244, Fvertebrobasilar18 × 20 × 173.0 × 2011basilar perforators1multi prior endovascular procedures; ↑ AN size on MRA6improved AN occl; slight filling at neck111
2369, MM113 × 13 × 122.75 × 1811M1 perforators1residual AN post-clipping3vessel remodeled; AN almost completely obliterated003
2456, FM125 × 18 × 173.25 × 35, 3.5 × 2011M1 perforators1TIA6>95% occl of AN006

AChA = anterior choroid artery; AICA = anterior inferior cerebellar artery; AN = aneurysm; FU = follow-up; HA = headache; Hx = history; multi = multiple; NA = not applicable; oblit = obliteration; occl = occlusion; OphA = ophthalmic artery; Tx = treatment; VA = vertebral artery; ↑ = increase; ↓ = decrease.

Aneurysm size is reported as the left to right, superior to inferior, and anterior to posterior dimensions, respectively.

Device size is reported as the diameter and length, respectively.

Two patients underwent 2 procedures. One patient had 2 PEDs placed on 2 occasions. The other patient underwent placement of 4 PEDs in the first procedure and 2 additional PEDs in the second procedure. Excluding these cases, 1–3 devices were placed in 22 patients (mean 1.8 devices). Multiple devices were placed in an overlapping fashion. The mean inflow vessel diameter was 3.3 mm (range 1.7–5.0 mm), and the mean outflow vessel diameter was 2.6 mm (range 1.5–4.5 mm). The mean length of normal vessel covered by the PED proximal to the aneurysm (“proximal purchase”) was 9.9 mm (range 4.4–17.0 mm). The “distal purchase” of the PED extending past the aneurysm into normal vessel was 7.6 mm (range 2.3–16.0 mm). Twenty-one (87.5%) of the 24 patients had perforator vessels or side branches covered by the PED. Fifteen had 1 PED covering the perforator, and 2 had 1–2 PEDs covering perforators (MCA) depending on where the overlapping component was. Three patients had 2 devices, and 1 patient had 3 PEDs covering a perforating vessel. Coils were added to supplement flow diversion in 2 cases. Dense packing was performed in one case and loose packing in another case. Postoperative imaging with angiography was performed in all cases with supplementary DynaCT performed in 8 cases. Three-dimensional angiography was performed in 1 case postoperatively.

Delivery of the PED(s) was successful in all cases without technical complication. Vessel wall apposition was achieved with the PED in all cases; however, 1 patient presented with a nonsignificant endoleak on follow-up angiography despite good vessel wall apposition. There was no significant in-stent thrombosis or significant thrombotic complication that required lysis intraoperatively. Twenty patients (83.3%) exhibited immediate new contrast stasis in the aneurysm following placement of the PED(s).

Complications

Twenty-three of 24 patients had no procedural complications (96%). One patient had a groin pseudoaneurysm that was managed conservatively. Of 24 patients, 4 (16.7%) had major complications related to aneurysm treatment and there was 1 death (4.2%). One patient died of cancer during the follow-up period.

Two patients with MCA aneurysms (Cases 9 and 20), and 1 patient with a basilar aneurysm (Case 19) had perforating vessel infarctions in the vascular territory of the region covered by the PED. One patient (Case 20) with an MCA aneurysm stopped taking clopidogrel without medical consultation at 5 months and his MCA PED became occluded, resulting in caudate, putamen, and cortical infarcts with associated hemiplegia. A 32-year-old man (Case 19) had an extremely complex case of a 46-mm basilar trunk aneurysm. He had undergone multiple stent-assisted coiling procedures at an outside institution; he presented to our institution with multiple cranial neuropathies and difficulty ambulating. After spanning the aneurysm with 4 PEDs he presented again with a thalamic infarct and worsening mass effect. Two further PEDs were placed in the proximal basilar artery; however, the aneurysm continued to fill. Despite further flow diversion, his clinical state declined, and he is bedridden and required percutaneous endoscopic gastrostomy tube placement and a tracheostomy. One patient (Case 1) with a 29-mm symptomatic cavernous aneurysm treated with 4 PEDs suffered a significant frontal intracerebral hemorrhage 1 week postoperatively and was discharged to a long-term care facility with hemiplegia and a percutaneous endoscopic gastrostomy tube.

Deaths

Two patients died. One patient (Case 14) was a 77-year-old man with progressive ataxia and a sixth cranial nerve palsy due to mass effect from a 23-mm basilar trunk aneurysm. Prior to PED placement a ventriculoperitoneal shunt was placed in preparation for the predicted swelling and aqueductal closure resulting from aneurysm thrombosis. He required bur hole drainage of a subdural hygroma following the shunt procedure. Once stabilized, the patient was given a loading dose of aspirin and clopidogrel for the PED placement. In an attempt to divert flow away from the aneurysm sac, a single PED was placed from the dominant vertebral artery across into the contralateral vertebral artery. Preoperative angiography demonstrated that the nondominant vertebral artery was only filling retrograde due to a chronic proximal occlusion. The patient initially did well; however, he presented at 7 months with a Hunt and Hess Grade V subarachnoid hemorrhage, and care was withdrawn by the family. He did not undergo angiography prior to his death. The other patient who died (Case 16), a 66-year-old man, was treated for a 25-mm M1 aneurysm that was found on imaging during a cancer workup. At the time of treatment he had an additional diagnosis of pancreatic cancer, and his oncologist predicted survival of 12 months at the time of considering treatment for his aneurysm. Given the reasonable prognosis for his cancer, the patient wished to have his aneurysm treated. Three PEDs were used to treat the aneurysm without complication, and the patient was discharged without complication or neurological deficit. Unfortunately, he died of metastatic pancreatic cancer 2 months after his procedure. He had no complications associated with the endovascular procedure at the time of death.

Angiographic Outcomes

Twenty-two of 24 patients had follow-up angiography available for review (mean follow-up 6.3 months, range 1 week to 12 months) (Table 5). One patient who died and another who refused to undergo follow-up did not undergo postoperative angiography. Seven (31.8%) had complete aneurysm occlusion, 6 (27.3%) had greater than 95% occlusion, 4 (18.2%) had a moderate decrease in size (50%–95%), 1 (4.55%) had a minimal decrease in size (< 50%), 3 (13.6%) had no change, and 1 (4.5%) had an increase in size.

TABLE 5:

Angiographic follow-up*

FindingNo. of Patients (%)
complete occlusion7 (31.8)
>95% occlusion6 (27.3)
moderate decrease (50–95%)4 (18.2)
minimal decrease (<50%)1 (4.5)
no change3 (13.6)
worse1 (4.5)

Angiographic follow-up was performed in 22 of the 24 patients.

Illustrative Cases

Case 15

This 73-year-old woman presented with diplopia and was found to have a fusiform 24-mm cavernous aneurysm. She was treated with a single 3.5 × 20–mm PED that spanned the entire diseased segment of the ICA. There was immediate intraaneurysmal contrast stasis (Fig. 1). The PED covered the ophthalmic artery; however, the vessel was noted to be filling immediately after placement of the device. The patient did have a small groin pseudoaneurysm that was managed conservatively. At the 6-month clinical and angiographic follow-up, the aneurysm was completely occluded and the cavernous ICA was remodeled. The ophthalmic artery was not filling from the ICA; however, collateral vessels from the external carotid artery were present. The patient's vision was normal, and the diplopia had resolved.

Fig. 1.
Fig. 1.

Case 15. A: Preoperative 3D rotational angiogram. B: Lateral unsubtracted radiograph obtained immediately postoperatively. The magnified inset shows the deployed PED with immediate contrast stasis in the aneurysm sac. C: Lateral projection DSA obtained 6 months postoperatively showing no residual aneurysm and ICA remodeling.

Case 23

This 69-year-old man presented after suffering a seizure while he was sleeping. He was found to have a complex distal M1 fusiform aneurysm that involved the MCA bifurcation (Fig. 2). Due to the complex involvement of the bifurcation, surgical clip reconstruction was performed. The aneurysm was noted to be particularly atheromatous. Intraoperative angiography demonstrated a residual aneurysm; however, further manipulation of the clips was not performed for fear of causing occlusion of perforators with thrombus. Follow-up angiography demonstrated an increase in the size of the lesion. Open surgical exploration was offered, but the patient declined further surgery. A single 2.75 × 18–mm PED was placed from the M1 to the trunk of a large M2 division. Radiological follow-up at 3 months revealed > 95% occlusion of the aneurysm, M1 remodeling, and no evidence on MRI of ischemic complications from covering the M1 perforators. At the 3-month clinical follow-up, the patient remains neurologically intact.

Fig. 2.
Fig. 2.

Case 23. A: Axial T2-weighted MR image demonstrating a large left MCA aneurysm with partial thrombus. B: Three-dimensional CT angiogram demonstrating the complex left MCA aneurysm that incorporates the MCA bifurcation. C: Preoperative left ICA Towne's projection DSA. D: Intraoperative angiogram demonstrating a residual aneurysm after a complex clip reconstruction. E: Towne's projection DSA obtained at the 6-month follow-up demonstrating a tiny residual aneurysm. F: Axial T2-weighted MR image obtained at the 6-month follow-up showing interim thrombosis of the aneurysm compared with that obtained preoperatively (A).

Case 21

This 26-year-old woman underwent screening with MRA because of a family history of aneurysms. A fusiform 5 × 5 × 5–mm M3 aneurysm was found on subsequent angiography (Fig. 3). The patient declined an open surgical approach with clip reconstruction. She was treated with a single 2.5 × 12–mm PED without complication. Angiographic follow-up at 6 months demonstrated complete aneurysm obliteration with normal filling of distal vasculature. She remains neurologically intact at 6 months.

Fig. 3.
Fig. 3.

Case 21. A: Preoperative left ICA lateral projection DSA demonstrating an M3 fusiform aneurysm. B: Immediate postoperative DSA showing stasis in the aneurysm sac after placement of the PED. C: Three-dimensional rotational CT angiography demonstrating the PED well placed across the length of the aneurysm. D: Six-month follow-up lateral projection DSA showing no residual aneurysm.

Case 3

This 74-year-old woman was previously treated for a fusiform V4 aneurysm with a stent coil procedure. An 11-mm recurrence of the aneurysm on follow-up angiography was found (Fig. 4). Two PEDs (4 × 14 mm and 3.75 × 20 mm) were placed with both devices overlapping and were noted to cover the posterior inferior cerebellar artery (PICA). Care was taken to achieve good endoluminal apposition by extending the coverage of the PEDs beyond both the proximal and distal limits of the old stent. The procedure was uncomplicated and at 6 months follow-up she remains neurologically intact. Angiography at 6 months demonstrated complete occlusion of the aneurysm, remodeling of the vertebral artery, and normal flow through the PICA.

Fig. 4.
Fig. 4.

Case 3. A: Lateral projection DSA demonstrating the complex previously stent-coiled V4 aneurysm. B: Preoperative 3D DSA demonstrating a complex previously stent-coiled V4 fusiform aneurysm with residual filling. C: Six-month follow-up unsubtracted radiograph showing the PEDs (2) spanning the coil mass and extending beyond the proximal and distal limits of the old stent. D: Six-month follow-up anteroposterior projection DSA demonstrating no residual aneurysm. Note that the PICA still fills despite being covered by 2 PEDs.

Case 24

This 56-year-old woman presented with a TIA secondary to a 25 × 18 × 17–mm fusiform M1 aneurysm. She was treated with a 3.25 × 35–mm and a 3.5 × 20–mm PED, as well as supplemental coiling using a “jailing” technique (Fig. 5). The coils were relatively tightly packed. Immediate stasis was noted in the aneurysm. The procedure was uncomplicated. Postoperatively, the patient did well and remained neurologically intact until the last clinical follow-up at 6 months. Angiographic follow-up at 6 months revealed a tiny amount of residual aneurysm (> 95% occlusion). All major efferent vessels were patent.

Fig. 5.
Fig. 5.

Case 24. A: Preoperative T2-weighted MR image demonstrating a large fusiform MCA aneurysm with components of thrombus. B: Preoperative anteroposterior projection DSA showing a complex fusiform aneurysm involving the entire M1. C: Three-dimensional reconstructed DSA showing the involvement of the M1 throughout its entire course. D: Postoperative radiograph demonstrating the placement of 2 PEDs spanning from the ICA into an M2 branch. Coils were used to supplement the flow diversion with the PEDs. E: Immediate postoperative 3D rotational CT angiogram showing the PED construct spanning the entire aneurysm from the ICA into a large M2 trunk, as well as the coil mass. F: Six-month follow-up Towne's progression DSA demonstrating a tiny residual aneurysm with parent vessel reconstruction.

Discussion

The treatment of fusiform aneurysms by open surgery or endovascular techniques remains a challenge for neurosurgeons.3,15,19,20 Open surgical management of these complex lesions is complicated by difficulties in visualizing perforating vessels, presence of atheroma, and challenges of surgical access in the cases of large posterior circulation aneurysms. Hunterian ligation is a relatively simple technique that has been used in an attempt to divert flow away from the aneurysm and to induce thrombosis.10 In the endovascular era this can be performed with parent vessel deconstruction using coil embolization. Hunterian ligation may be effective at decreasing flow and may indeed result in flow reversal and shrinkage of the aneurysm. If flow is diminished too much then complex bypass techniques may need to be used to prevent ischemic complications.8,14

Treatment of fusiform aneurysms with endovascular flow diversion has been limited to a discussion in small case series or as a subgroup in larger series of all aneurysm types.2,4,7,17,19,21 In a series by Siddiqui et al.,22 7 patients underwent flow diversion for large or giant fusiform vertebrobasilar aneurysms. The PED was used in 6 patients, and the Silk (Balt Extrusion) device was used in 1 patient. At last clinical follow-up 4 patients had died and the other 3 had severe disability (mRS Score 5).22 Klisch et al.11 reported 2 cases of flow diversion for large fusiform basilar trunk aneurysms. In both cases the aneurysm was nearly completely obliterated at follow-up; however, both patients had stent thrombosis after stopping clopidogrel after 1 year. One patient died and the other underwent successful urgent revascularization.11 Kan et al.9 reported a multicenter US study; 62 PED procedures were performed to treat 58 aneurysms in 56 patients. Ninety percent of the aneurysms were saccular. Four of the 8 vertebrobasilar aneurysms were fusiform, and 1 of these patients suffered a perforator infarction with resultant permanent neurological deficit after placement of a flow diverter. In the current series 59.1% of cases demonstrated complete or > 95% occlusion on follow-up angiography. An additional 18.2% had 50%–95% decrease in aneurysm size. From a clinical standpoint 82.6% of patients did well: 2 patients improved (8.7%), 17 remained stable (73.9%), 3 worsened (13.0%), and 1 died (4.3%). Experience from our group is similar to previous studies and suggests that in selected patients flow diversion using the PED is a reasonable treatment option.

The concept of flow diversion in the setting of compressive symptoms is intuitive. Decreasing the mass effect of a partially thrombosed aneurysm with flow diversion without the placement of additional coil mass has been used to relieve pressure on surrounding neural elements. In a series of 30 aneurysms (3 fusiform), Szikora et al. demonstrated significant improvement in symptoms due to mass effect from large aneurysms treated with flow diversion.23 In their series 6 patients had vision loss, 10 had double vision, and 1 had brainstem compression and hemiparesis. At follow-up, vision loss had improved in 9 of 10 patients, and double vision completely resolved in 7 of 10 and partially in an additional 3 patients. The patient with hemiparesis became asymptomatic.23 Clinical improvements in cranial neuropathies due to aneurysm mass effect were not borne out in our series. Four patients in this series primarily presented with cranial neuropathy as a result of the compressive effects of the aneurysm. Of these, 2 patients are in a long-term care facility with significant disability (follow-up angiography in both cases demonstrated < 50% aneurysm occlusion), 1 patient has had stable diplopia (follow-up angiogram demonstrated > 95% occlusion), and the remaining patient has had resolution of diplopia (angiography demonstrated 100% occlusion). The less than satisfactory outcomes in these patients should be taken in the context that we treated only a small number of patients in our series for symptoms of mass effect or compression. In addition, the lesions treated in these patients were of a particularly complex nature, and salvage therapy was performed in 1 case following multiple stent and coiling procedures at an outside institution.

Remodeling (> 95% aneurysm obliteration) of the parent vessel to close to a normal anatomical configuration occurred in 59.1% of cases in this series. A moderate decrease (50%–95%) in aneurysm size was seen in an additional 18.2%, yielding significant angiographic improvement in 77.3% of cases. In the current series 21 of 24 patients had PEDs that covered perforating vessels (87.5%), including large vessels such as the ophthalmic artery and PICA. Of those patients with PEDs covering perforators, 2 patients (8.3%; one with a basilar trunk aneurysm and the other with an M1 aneurysm) had symptomatic perforator infarctions during the follow-up period despite continuing dual antiplatelet therapy with aspirin and clopidogrel. One device was placed in the patient with an M1 aneurysm, and a total of 6 devices were placed in the patient with the giant basilar trunk aneurysm. Phillips et al. treated 32 posterior circulation aneurysms with the PED but reported perforator infarctions in 14%, with a permanent morbidity of 9.4%.16 In this current series, only 1 case (a symptomatic cavernous aneurysm) of a large perforating vessel was seen to be occluded (ophthalmic artery) at angiographic follow-up after initially filling immediately post-stenting. The patient was not symptomatic, and at follow-up the collaterals from the external carotid artery continued to perfuse the orbital contents; the patient's vision remained normal. This finding is similar to that in previous studies in which the ophthalmic artery was occluded by the PED. Puffer et al. examined the patency of the ophthalmic artery after placement of 1–3 PEDs for 20 paraclinoid aneurysms.18 The authors found that the mean number of PEDs in the patients with change in flow or occluded ophthalmic arteries was 2.4 compared with 1.9 in the patients with no change in flow in the ophthalmic artery (p = 0.09). At angiographic follow-up normal antegrade flow was seen in 68% of patients and slow flow in 11% of patients. The ophthalmic artery was occluded in 21% of cases; however, no patient developed clinical sequelae as a result of ophthalmic artery occlusion due to the development of collateral vessels.18 One patient in our series had a thrombus in the MCA (and MCA aneurysm) that caused a stroke after self-discontinuing his dual antiplatelet therapy prior to angiographic follow-up. Such cases illustrate the need for patient education and compliance with regard to the importance of antiplatelet medications. The optimal regimen for antiplatelet therapy in the use of the PED is physician dependent, and currently there is a lack of clear guidelines. We favor dual antiplatelet therapy until follow-up angiography (usually at 6 months initially) demonstrates that the parent vessel is completely remodeled and the aneurysm is occluded. Following this, the patient is kept on a regimen of 81 mg daily aspirin for life. Several groups advise stopping aspirin therapy completely. While the number of cases in this series and others is too small to draw any firm conclusions, we recommend avoiding using overlapping multiple devices in the MCA and basilar trunk. Placement of overlapping devices in these regions where the perforators are small and of relatively low-flow demand places the patient at risk for ischemic complications.

Two patients were treated with the PED as salvage treatment for residual aneurysm following clipping of complex M1 aneurysms. Both patients had greater than 95% aneurysm obliteration at angiographic follow-up; however, 1 patient suffered a perforator stroke. This patient made a good recovery and at 12 months of follow-up is neurologically intact. Such cases illustrate the benefits of a multidisciplinary approach to the management of complex cases, and the PED can be a useful option in cases of residual aneurysm.

Conclusions

This series of endovascular treatment for fusiform cerebral aneurysms with flow diversion represents the largest series of its type. At last follow-up, angiographic improvement was seen in more than 80% of cases, with complete or greater than 95% aneurysm obliteration in 59.1% of the cases. Given the complex nature of the aneurysms treated, the complication rates were acceptable. Eighty-three percent of patients did well after the procedure and were neurologically stable or improved after intervention. Overall, in this series endovascular treatment of fusiform aneurysms with flow diversion appears to be a safe and effective treatment. Further larger studies will be needed to determine the absolute risk of perforator occlusion in the regions of the MCA and basilar trunk. Fusiform aneurysms of the basilar trunk remain a therapeutic challenge.

Disclosure

Drs. Dumont and Jabbour are consultants for ev3.

Author contributions to the study and manuscript preparation include the following. Conception and design: Jabbour, Monteith, Tsimpas, Dumont, Gonazalez, Rosenwasser. Acquisition of data: all authors. Analysis and interpretation of data: Jabbour, Monteith, Dumont, Tjoumakaris, Gonazalez, Rosenwasser. Drafting the article: Jabbour, Monteith, Tsimpas. Critically revising the article: all authors. Reviewed submitted version of manuscript: all authors. Approved the final version of the manuscript on behalf of all authors: Jabbour. Administrative/technical/material support: Jabbour.

This article contains some figures that are displayed in color online but in black-and-white in the print edition.

References

  • 1

    Anson JALawton MTSpetzler RF: Characteristics and surgical treatment of dolichoectatic and fusiform aneurysms. J Neurosurg 84:1851931996

  • 2

    Briganti FNapoli MTortora FSolari DBergui MBoccardi E: Italian multicenter experience with flow-diverter devices for intracranial unruptured aneurysm treatment with periprocedural complications—a retrospective data analysis. Neuroradiology 54:114511522012

  • 3

    Chen PRAbla AAMcDougall CGSpetzler RFAlbuquerque FC: Surgical techniques for unclippable fusiform A2-anterior cerebral artery aneurysms and description of a frontopolar-to-A2 bypass. World Neurosurg [epub ahead of print]2012

  • 4

    Chitale RGonzalez LFRandazzo CDumont ASTjoumakaris SRosenwasser R: Single center experience with pipeline stent: feasibility, technique, and complications. Neurosurgery 71:6796912012

  • 5

    Drake CGPeerless SJ: Giant fusiform intracranial aneurysms: review of 120 patients treated surgically from 1965 to 1992. J Neurosurg 87:1411621997

  • 6

    Drake CGPeerless SJFerguson GG: Hunterian proximal arterial occlusion for giant aneurysms of the carotid circulation. J Neurosurg 81:6566651994

  • 7

    Fiorella DWoo HHAlbuquerque FCNelson PK: Definitive reconstruction of circumferential, fusiform intracranial aneurysms with the pipeline embolization device. Neurosurgery 62:111511212008

  • 8

    Kalani MYZabramski JMNakaji PSpetzler RF: Bypass and flow reduction for complex basilar and vertebrobasilar junction aneurysms. Neurosurgery 72:7637762013

  • 9

    Kan PSiddiqui AHVeznedaroglu ELiebman KMBinning MJDumont TM: Early postmarket results after treatment of intracranial aneurysms with the pipeline embolization device: a U.S. multicenter experience. Neurosurgery 71:108010882012

  • 10

    Kellner CPHaque RMMeyers PMLavine SDConnolly ES JrSolomon RA: Complex basilar artery aneurysms treated using surgical basilar occlusion: a modern case series. Clinical article. J Neurosurg 115:3193272011

  • 11

    Klisch JTurk ATurner RWoo HHFiorella D: Very late thrombosis of flow-diverting constructs after the treatment of large fusiform posterior circulation aneurysms. AJNR Am J Neuroradiol 32:6276322011

  • 12

    Lylyk PMiranda CCeratto RFerrario AScrivano ELuna HR: Curative endovascular reconstruction of cerebral aneurysms with the pipeline embolization device: the Buenos Aires experience. Neurosurgery 64:6326432009

  • 13

    Nelson PKLylyk PSzikora IWetzel SGWanke IFiorella D: The pipeline embolization device for the intracranial treatment of aneurysms trial. AJNR Am J Neuroradiol 32:34402011

  • 14

    Nussbaum ESMendez ACamarata PSebring L: Surgical management of fusiform aneurysms of the peripheral posteroinferior cerebellar artery. Neurosurgery 53:8318352003

  • 15

    Phatouros CCSasaki TYHigashida RTMalek AMMeyers PMDowd CF: Stent-supported coil embolization: the treatment of fusiform and wide-neck aneurysms and pseudoaneurysms. Neurosurgery 47:1071152000

  • 16

    Phillips TJWenderoth JDPhatouros CCRice HSingh TPDevilliers L: Safety of the pipeline embolization device in treatment of posterior circulation aneurysms. AJNR Am J Neuroradiol 33:122512312012

  • 17

    Piano MValvassori LQuilici LPero GBoccardi E: Midterm and long-term follow-up of cerebral aneurysms treated with flow diverter devices: a single-center experience. Special topic. J Neurosurg 118:4084162013

  • 18

    Puffer RCKallmes DFCloft HJLanzino G: Patency of the ophthalmic artery after flow diversion treatment of paraclinoid aneurysms. Clinical article. J Neurosurg 116:8928962012

  • 19

    Raphaeli GCollignon LDe Witte OLubicz B: Endovascular treatment of posterior circulation fusiform aneurysms: single-center experience in 31 patients. Neurosurgery 69:2742832011

  • 20

    Rey-Dios RCohen-Gadol AA: Microsurgical treatment of fusiform middle cerebral artery aneurysms: technique. Neurosurgery 73:1 Suppl Operativeons22013. (Video)

  • 21

    Saatci IYavuz KOzer CGeyik SCekirge HS: Treatment of intracranial aneurysms using the pipeline flow-diverter embolization device: a single-center experience with long-term follow-up results. AJNR Am J Neuroradiol 33:143614462012

  • 22

    Siddiqui AHAbla AAKan PDumont TMJahshan SBritz GW: Panacea or problem: flow diverters in the treatment of symptomatic large or giant fusiform vertebrobasilar aneurysms. Clinical article. J Neurosurg 116:125812662012

  • 23

    Szikora IMarosfoi MSalomváry BBerentei ZGubucz I: Resolution of mass effect and compression symptoms following endoluminal flow diversion for the treatment of intracranial aneurysms. AJNR Am J Neuroradiol 34:9359392013

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Article Information

Address correspondence to: Pascal Jabbour, M.D., Division of Neurovascular Surgery and Endovascular Neurosurgery, Thomas Jefferson University Hospital, Third Floor, 909 Walnut St., Philadelphia, PA 19107. email: pascal.jabbour@jefferson.edu.

Please include this information when citing this paper: published online January 24, 2014; DOI: 10.3171/2013.12.JNS13945.

© AANS, except where prohibited by US copyright law.

Headings

Figures

  • View in gallery

    Case 15. A: Preoperative 3D rotational angiogram. B: Lateral unsubtracted radiograph obtained immediately postoperatively. The magnified inset shows the deployed PED with immediate contrast stasis in the aneurysm sac. C: Lateral projection DSA obtained 6 months postoperatively showing no residual aneurysm and ICA remodeling.

  • View in gallery

    Case 23. A: Axial T2-weighted MR image demonstrating a large left MCA aneurysm with partial thrombus. B: Three-dimensional CT angiogram demonstrating the complex left MCA aneurysm that incorporates the MCA bifurcation. C: Preoperative left ICA Towne's projection DSA. D: Intraoperative angiogram demonstrating a residual aneurysm after a complex clip reconstruction. E: Towne's projection DSA obtained at the 6-month follow-up demonstrating a tiny residual aneurysm. F: Axial T2-weighted MR image obtained at the 6-month follow-up showing interim thrombosis of the aneurysm compared with that obtained preoperatively (A).

  • View in gallery

    Case 21. A: Preoperative left ICA lateral projection DSA demonstrating an M3 fusiform aneurysm. B: Immediate postoperative DSA showing stasis in the aneurysm sac after placement of the PED. C: Three-dimensional rotational CT angiography demonstrating the PED well placed across the length of the aneurysm. D: Six-month follow-up lateral projection DSA showing no residual aneurysm.

  • View in gallery

    Case 3. A: Lateral projection DSA demonstrating the complex previously stent-coiled V4 aneurysm. B: Preoperative 3D DSA demonstrating a complex previously stent-coiled V4 fusiform aneurysm with residual filling. C: Six-month follow-up unsubtracted radiograph showing the PEDs (2) spanning the coil mass and extending beyond the proximal and distal limits of the old stent. D: Six-month follow-up anteroposterior projection DSA demonstrating no residual aneurysm. Note that the PICA still fills despite being covered by 2 PEDs.

  • View in gallery

    Case 24. A: Preoperative T2-weighted MR image demonstrating a large fusiform MCA aneurysm with components of thrombus. B: Preoperative anteroposterior projection DSA showing a complex fusiform aneurysm involving the entire M1. C: Three-dimensional reconstructed DSA showing the involvement of the M1 throughout its entire course. D: Postoperative radiograph demonstrating the placement of 2 PEDs spanning from the ICA into an M2 branch. Coils were used to supplement the flow diversion with the PEDs. E: Immediate postoperative 3D rotational CT angiogram showing the PED construct spanning the entire aneurysm from the ICA into a large M2 trunk, as well as the coil mass. F: Six-month follow-up Towne's progression DSA demonstrating a tiny residual aneurysm with parent vessel reconstruction.

References

1

Anson JALawton MTSpetzler RF: Characteristics and surgical treatment of dolichoectatic and fusiform aneurysms. J Neurosurg 84:1851931996

2

Briganti FNapoli MTortora FSolari DBergui MBoccardi E: Italian multicenter experience with flow-diverter devices for intracranial unruptured aneurysm treatment with periprocedural complications—a retrospective data analysis. Neuroradiology 54:114511522012

3

Chen PRAbla AAMcDougall CGSpetzler RFAlbuquerque FC: Surgical techniques for unclippable fusiform A2-anterior cerebral artery aneurysms and description of a frontopolar-to-A2 bypass. World Neurosurg [epub ahead of print]2012

4

Chitale RGonzalez LFRandazzo CDumont ASTjoumakaris SRosenwasser R: Single center experience with pipeline stent: feasibility, technique, and complications. Neurosurgery 71:6796912012

5

Drake CGPeerless SJ: Giant fusiform intracranial aneurysms: review of 120 patients treated surgically from 1965 to 1992. J Neurosurg 87:1411621997

6

Drake CGPeerless SJFerguson GG: Hunterian proximal arterial occlusion for giant aneurysms of the carotid circulation. J Neurosurg 81:6566651994

7

Fiorella DWoo HHAlbuquerque FCNelson PK: Definitive reconstruction of circumferential, fusiform intracranial aneurysms with the pipeline embolization device. Neurosurgery 62:111511212008

8

Kalani MYZabramski JMNakaji PSpetzler RF: Bypass and flow reduction for complex basilar and vertebrobasilar junction aneurysms. Neurosurgery 72:7637762013

9

Kan PSiddiqui AHVeznedaroglu ELiebman KMBinning MJDumont TM: Early postmarket results after treatment of intracranial aneurysms with the pipeline embolization device: a U.S. multicenter experience. Neurosurgery 71:108010882012

10

Kellner CPHaque RMMeyers PMLavine SDConnolly ES JrSolomon RA: Complex basilar artery aneurysms treated using surgical basilar occlusion: a modern case series. Clinical article. J Neurosurg 115:3193272011

11

Klisch JTurk ATurner RWoo HHFiorella D: Very late thrombosis of flow-diverting constructs after the treatment of large fusiform posterior circulation aneurysms. AJNR Am J Neuroradiol 32:6276322011

12

Lylyk PMiranda CCeratto RFerrario AScrivano ELuna HR: Curative endovascular reconstruction of cerebral aneurysms with the pipeline embolization device: the Buenos Aires experience. Neurosurgery 64:6326432009

13

Nelson PKLylyk PSzikora IWetzel SGWanke IFiorella D: The pipeline embolization device for the intracranial treatment of aneurysms trial. AJNR Am J Neuroradiol 32:34402011

14

Nussbaum ESMendez ACamarata PSebring L: Surgical management of fusiform aneurysms of the peripheral posteroinferior cerebellar artery. Neurosurgery 53:8318352003

15

Phatouros CCSasaki TYHigashida RTMalek AMMeyers PMDowd CF: Stent-supported coil embolization: the treatment of fusiform and wide-neck aneurysms and pseudoaneurysms. Neurosurgery 47:1071152000

16

Phillips TJWenderoth JDPhatouros CCRice HSingh TPDevilliers L: Safety of the pipeline embolization device in treatment of posterior circulation aneurysms. AJNR Am J Neuroradiol 33:122512312012

17

Piano MValvassori LQuilici LPero GBoccardi E: Midterm and long-term follow-up of cerebral aneurysms treated with flow diverter devices: a single-center experience. Special topic. J Neurosurg 118:4084162013

18

Puffer RCKallmes DFCloft HJLanzino G: Patency of the ophthalmic artery after flow diversion treatment of paraclinoid aneurysms. Clinical article. J Neurosurg 116:8928962012

19

Raphaeli GCollignon LDe Witte OLubicz B: Endovascular treatment of posterior circulation fusiform aneurysms: single-center experience in 31 patients. Neurosurgery 69:2742832011

20

Rey-Dios RCohen-Gadol AA: Microsurgical treatment of fusiform middle cerebral artery aneurysms: technique. Neurosurgery 73:1 Suppl Operativeons22013. (Video)

21

Saatci IYavuz KOzer CGeyik SCekirge HS: Treatment of intracranial aneurysms using the pipeline flow-diverter embolization device: a single-center experience with long-term follow-up results. AJNR Am J Neuroradiol 33:143614462012

22

Siddiqui AHAbla AAKan PDumont TMJahshan SBritz GW: Panacea or problem: flow diverters in the treatment of symptomatic large or giant fusiform vertebrobasilar aneurysms. Clinical article. J Neurosurg 116:125812662012

23

Szikora IMarosfoi MSalomváry BBerentei ZGubucz I: Resolution of mass effect and compression symptoms following endoluminal flow diversion for the treatment of intracranial aneurysms. AJNR Am J Neuroradiol 34:9359392013

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