Article Text
Abstract
Background and purpose Endovascular treatment (EVT) has emerged as an alternative therapeutic strategy for the treatment of intracranial fusiform aneurysms (IFAs), but little is known about the safety and efficacy of deconstructive and reconstructive methods, especially in patients presenting with subarachnoid hemorrhage (SAH). The purpose of this study is to describe the radiological and clinical outcomes in patients with IFAs undergoing EVT.
Methods A retrospective analysis was conducted of 18 patients undergoing EVT of IFAs, 13 of whom (72.2%) presented with SAH. Radiological outcomes were characterized by the presence of parent vessel opacification and aneurysmal remnants for patients undergoing deconstructive and reconstructive EVT, respectively. Clinical outcomes were characterized by the Glasgow Outcome Scale. Contingency analysis of factors associated with clinical outcomes in patients with ruptured aneurysms was conducted.
Results Technical success was achieved in 17 of the 18 patients (94.4%), with 10 (55.6%) undergoing reconstructive EVT and eight (44.4%) undergoing deconstructive EVT. For patients with SAH, favorable clinical outcomes were achieved in 9/13 (69.2%), with 3/6 (50.0%) undergoing reconstructive EVT and 6/7 (85.7%) undergoing deconstructive EVT. Among patients with ruptured aneurysms, only Hunt–Hess grade ≥3 was associated with an unfavorable clinical outcome (p=0.007). Favorable clinical outcomes were seen in all five patients with unruptured aneurysms.
Conclusion Both deconstructive and reconstructive EVT were found to be safe and effective in patients with unruptured aneurysms. Reconstructive EVT may be associated with a higher incidence of poor clinical outcomes in patients presenting with high-grade SAH.
- Endovascular
- subarachnoid hemorrhage
- intracranial fusiform aneurysm
- outcomes
- aneurysm
- intervention
- artery
- temporal bone
- MRI
- CT
- subarachnoid
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- Endovascular
- subarachnoid hemorrhage
- intracranial fusiform aneurysm
- outcomes
- aneurysm
- intervention
- artery
- temporal bone
- MRI
- CT
- subarachnoid
Introduction
Aneurysmal subarachnoid hemorrhage (SAH) is associated with high mortality and poor outcomes. Despite declining case fatality rates over the last three decades, mortality from aneurysmal SAH continues to be high with 1-month mortality ranging from 18% to 57%.1 Most cases of non-traumatic SAH are caused by ruptured saccular aneurysms with <5% secondary to ruptured fusiform intracranial aneurysms.2 The fusiform shape seen on angiography can be secondary to arterial dissection or atherosclerosis.3 While less common than saccular aneurysms, the presence of unruptured fusiform aneurysms have a poor prognosis of up to 80% mortality in 5 years if left untreated.4 The characteristics of these aneurysms that make treatment more difficult include the lack of a defined neck region to exclude from the parent artery and the relatively high frequency of normal perforating arteries originating from the aneurysm.
Although fusiform intracranial aneurysms can be managed surgically, endovascular treatment (EVT) has emerged as an alternative therapeutic strategy. EVT of fusiform aneurysms is performed using deconstructive or reconstructive strategies. Deconstructive EVT refers to the occlusion of the parent vessel through embolic techniques whereas reconstructive treatment is characterized by the use of stents and/or coils to occlude the diseased portion of the vessel while preserving a parent artery lumen.
The lack of standard protocols for the treatment of fusiform intracranial aneurysms is most probably secondary to highly variable clinical presentations of patients with such radiographic findings and the relative rarity of this condition. In this study we report the immediate and long-term clinical and radiographic findings in patients who have undergone deconstructive or reconstructive EVT of fusiform intracranial aneurysms.
Methods
Patient population and clinical features
Between August 2005 and July 2011, 18 patients (10 men) of mean age 48.2 years (range 20–83) underwent EVT for fusiform aneurysms (tables 1 and 2). Longitudinal angiographic follow-up data, defined as angiography performed at 2 months post-intervention or later, were available for 7/15 patients (46.7%) surviving the initial intervention with a mean follow-up time of 13.2 months (range 3–36, 95% CI 6.54 to 19.9). Longitudinal clinical data, defined as clinical examination conducted at 2 months post-intervention or later, were available for 2/10 patients (20%) with SAH and 3/5 patients (60.0%) with unruptured aneurysms surviving the initial intervention. Mean clinical follow-up time was 14.0 months (range 2–42, 95% CI 7.34 to 20.7).
The diagnosis of SAH was based on clinical history and non-enhanced CT (NECT) scan of the head and was clinically graded using the Hunt–Hess (H/H) grading system. Of the 18 patients in the study, 13 presented with SAH while the other five underwent elective aneurysm repair after having undergone prior radiologic examinations that revealed these unruptured aneurysms. Four of these patients were felt to have asymptomatic aneurysms. One patient had headache thought to be related to aneurysm despite negative NECT.
Aneurysm treatment
All patients were treated using reconstructive or deconstructive EVT without adjunctive open surgical therapy. Reconstructive treatment involved the use of stents and/or stent-assisted coiling for aneurysm repair. Most patients undergoing stent placement were pretreated with clopidogrel and aspirin. Patients received 75 mg clopidogrel daily for 7 days before the procedure if undergoing repair of unruptured aneurysms or 300–450 mg immediately before the procedure if undergoing repair of ruptured aneurysms. Patient 1 was pretreated with 10 mg abxicimab instead of clopidogrel. All patients were systemically heparinized immediately prior to stent placement. Deconstructive therapy was performed using either n-butyl cyanoacrylate (nBCA) or bare metal coils. All procedures were conducted under general anesthesia except for patient 14 in whom the procedure which was done under conscious sedation with intra-arterial sodium amytal testing. Digital subtraction angiography (DSA) with conventional projections and three-dimensional rotational angiography was performed.
Clinical and angiographic evaluation
Clinical outcomes at hospital discharge were characterized using the Glasgow Outcome Scale.5 For the purposes of analysis and reporting, the Glasgow Outcome Scale was dichotomized as favorable (moderate disability or good recovery) or unfavorable (severe disability, vegetative state, dead).
All patients underwent conventional DSA for diagnosis and treatment of aneurysms. Intraprocedural complications were reported. Immediate angiographic outcomes after deconstructive or reconstructive EVT were characterized by the presence of distal opacification or aneurysmal remnants, respectively. Long-term angiographic follow-up with either conventional angiography or magnetic resonance angiography (MRA) was performed at variable intervals depending on the initial clinical presentation and subsequent longitudinal clinical course. Long-term outcomes were described based on angiographic findings including recanalization, in stent-stenosis and the need for further interventions.
Statistical analysis
An exploratory cross-table analysis of factors associated with clinical outcomes in patients presenting with ruptured aneurysms was conducted using Fisher exact test with p<0.05 being the threshold for statistical significance (table 3). Independent variables included gender, H/H grade ≥3, reconstructive EVT, hypertension, diabetes and a history of smoking. SPSS V.15.0 was used for statistical analysis.
Results
Immediate post-procedure angiographic and clinical outcomes
Angiography performed immediately after the procedure showed that 17/18 aneurysms (94.4%) were successfully treated, 10 (55.6%) being treated with reconstructive EVT and eight (44.4%) with deconstructive EVT. The only patient with an unsuccessfully treated aneurysm had decreased but significant opacification of the aneurysm despite efforts of stent-assisted coiling complicated by proximal parent vessel dissection (patient 4).
Favorable clinical outcomes were achieved in 7/10 patients (70%) undergoing reconstructive EVT and 7/8 patients (87.5%) undergoing deconstructive EVT. Among patients with good clinical outcomes, no periprocedural complications occurred at the time of the intervention and no neurologic deficits were seen at discharge. All four patients experiencing a poor outcome presented with SAH of H/H ≥3. Three of these four patients died (patients 1, 2 and 4) while one (patient 9) was discharged with severe functional disability requiring assistance with activities of daily living.
In two of the patients who died, rupture of the aneurysm occurred during reconstructive EVT. In patient 1 the rupture occurred prior to coil deployment during stent-assisted coiling of a second segment of the anterior cerebral artery (A2) aneurysm. Despite technical success being achieved with no further angiographic evidence of aneurysmal remnant or extravasation of contrast after EVT, the patient deteriorated clinically and care was withdrawn after 48 h. In patient 2 the rupture occurred immediately after coil deployment during stent-assisted coiling of a posterior cerebral artery (PCA) aneurysm. Again, despite technical success, the patient deteriorated clinically over the subsequent 12 h before care was withdrawn.
The third patient who died (patient 4) underwent unsuccessful stent-assisted coiling of a ruptured basilar artery fusiform aneurysm complicated by left vertebral artery dissection. This patient experienced subsequent neurologic decline characterized by waxing and waning mental status. Care was withdrawn after the patient developed nosocomial pneumonia with worsening cardiopulmonary status but without aneurysmal re-rupture.
Statistical analysis of factors associated with clinical outcome at discharge among patients with ruptured aneurysms shows that only the presence of H/H grade ≥3 was associated with an unfavorable clinical outcome (table 3).
Long-term angiographic and clinical outcomes
Long-term angiographic outcomes were available for 7/15 patients (46.7%) who survived after the initial intervention, with all five patients with unruptured aneurysms and 2/13 (15.4%) with SAH having angiographic follow-up. Of the five patients with unruptured aneurysms, one had an incompletely treated aneurysm while another patient experienced recanalization. A small aneurysmal remnant was noted in patient 14 immediately after treatment with stability noted at follow-up at 10, 18 and 30 months post-procedure. Patient 15, who initially underwent stent-assisted coiling of a vertebrobasilar aneurysm, experienced recanalization of an aneurysm at 6 months requiring additional coil placement. Subsequent follow-up at 18 months showed growth of the original aneurysm remnant necessitating an additional stent-assisted coiling procedure which was without complication.
In the two patients with SAH and follow-up angiographic results, both underwent reconstructive EVT with one patient undergoing stent-assisted coiling (patient 3) and another patient undergoing placement of two stents without coils (patient 5). No evidence of recanalization was noted at 24 and 36 months follow-up for patient 3 and at 12 months for patient 5.
Long-term clinical follow-up data were available for 3/5 patients (60.0%) undergoing elective EVT for unruptured fusiform aneurysms and 2/10 patients (20.0%) undergoing EVT after SAH. All patients presenting for follow-up clinic appointments were found to be stable with no neurologic deficits (table 2).
Representative cases
Case 1
Case 1 (patient 7) was a previously healthy 35-year-old woman who presented with headache of 2 days duration. A CT scan of the head demonstrated findings consistent with SAH. On angiography, a fusiform aneurysm of the right superior cerebellar artery was noted (figure 1A,B). This aneurysm was treated with four Berenstein liquid coils (figure 1C) followed by nBCA embolization (figure 1D). The procedure was technically successful; however, a small amount of glue material was seen to reflux into the first segment (P1) and third segment of the right PCA, with no flow limitations or clinical sequelae (figure 1E). The patient was given a heparin bolus and placed on a heparin drip for 24 h. At follow-up clinical examination 24 h after the procedure she was found to be asymptomatic with no neurologic or functional deficits.
Case 2
Case 2 (patient 14) was a 64-year-old hypertensive with a history of chronic retro-orbital headache unresponsive to medical treatment. MRA was performed, which showed an unruptured left PCA fusiform aneurysm. Catheter angiography was performed under conscious sedation and confirmed the presence of a left first and second segment (P2) PCA aneurysm (figure 2A,B). A balloon test occlusion of the left PCA proximal to the aneurysm resulted in the patient experiencing right hemianopsia. One month later the patient underwent reconstructive endovascular repair of the fusiform aneurysm. Staged placement of a Neuroform-3 3.0×20 mm stent across the PCA aneurysm neck was performed without complications (figure 2C). MRA was performed after stent placement to assess the location of the stent in the lumen of fusiform aneurysm (figure 2D). Three weeks later the patient underwent completion coiling of the aneurysm without complication (figure 2E,F). The patient was found to be neurologically intact at follow-up visits at 12, 24 and 36 months. Angiography immediately after coiling showed evidence of a small aneurysmal remnant which remained stable at subsequent angiographic follow-up at 10, 18 and 30 months (figure 2E).
Case 3
Case 3 (patient 1) was a 50-year-old who experienced sudden onset of headache prior to losing consciousness. A CT scan of the head showed evidence of SAH, intraventricular hemorrhage and mild hydrocephalus. The patient was transferred to the neurosurgical intensive care unit where an emergency ventriculostomy drain was placed; however, the patient did not show improvement after drain placement and was subsequently taken to the angiography suite. Angiography showed a left A2 fusiform (figure 3A,B). A microcatheter was navigated into the largest portion of the aneurysm with plans to jail the microcatheter with the use of a stent. A Neuroform-3 2.5×15 mm stent was successfully placed across the segment of fusiform. A coil was successfully placed through the microcatheter in its intended location without herniation into the parent vessel; however, immediate DSA run after coil placement showed extravasation of contrast into the subarachnoid space (figure 3C). The patient became bradycardic and hypertensive and the ventriculostomy began to drain frank blood. The subarachnoid space and aneurysm were embolized with parent vessel patency preserved (figure 3D,E). A CT scan immediately afterwards showed extensive intraventricular hemorrhage, hydrocephalus and contrast extravasation into the intraventricular and subarachnoid space. The patient experienced neurologic decline over the subsequent 12 h, prompting a decision by the patient's family to withdraw care.
Discussion
Our analysis of patients with fusiform intracranial aneurysms shows a higher incidence of intraprocedural complications, mortality and poor clinical outcomes in patients undergoing reconstructive EVT than in those undergoing deconstructive EVT. In particular, this study shows that reconstructive endovascular therapy was associated with higher mortality among patients with high-grade SAH, whereas no mortalities were seen in patients with grade 1 SAH or those with non-ruptured aneurysms. Furthermore, in three of the four cases resulting in a poor clinical outcome, intraprocedural complications occurred and the patients decompensated either during or shortly after the time of reconstructive EVT.
Despite the high incidence of mortality and poor clinical outcome, reconstructive EVT has the potential to be safe and efficacious. While a larger proportion of patients undergoing reconstructive EVT experienced a poor clinical outcome than those undergoing deconstructive EVT, poor outcomes were only seen in patients with high-grade SAH. This finding suggests that reconstructive EVT may not be appropriate for this subgroup of patients.
Ultimately, the decision to pursue reconstructive or deconstructive EVT for fusiform intracranial aneurysms must weigh the potential risks and benefits of each method, with the choice of treatment being tailored to the patient depending on the aneurysm location, presence or absence of SAH and consideration of the vascular territory supplied by the diseased vessel. Deconstructive EVT allows for a relatively straightforward approach to treatment of these aneurysms, but at the expense of potential neurologic deficits secondary to occlusion of the parent vessel. The risks of secondary ischemia can be profound, especially in the vertebrobasilar vascular territory where brainstem function could be compromised through such treatment. As such, reconstructive EVT may be the only viable endovascular approach to management of aneurysms in which parent vessel occlusion may lead to serious neurologic deficits. Previous studies have shown mortality rates of 0–20% for reconstructive EVT in the repair of fusiform aneurysms, including the use of stents and/or coils.6–8 The mortality rates for reconstructive therapy compare favorably with the natural history of aneurysms where follow-up mortality may be as high as 40%.9
In the current study the mortality rate for reconstructive EVT was 30% (3/10). While this rate is higher than that of previously reported studies, it is important to note that, unlike previous studies, the majority of patients in this study undergoing reconstructive EVT presented with SAH. Furthermore, all three patients who died presented with SAH of H/H grade ≥3. While no deaths were seen in the group of patients undergoing deconstructive EVT, the only poor outcome seen among this group was in a patient presenting with SAH of H/H grade 3. The association between poor clinical outcome and high-grade SAH was found to be statistically significant. This finding is consistent with a previous study which showed that low H/H grade is a predictor of favorable clinical outcome in patients undergoing deconstructive EVT.10 To our knowledge, there have been no previous studies assessing predictors of outcome in patients undergoing reconstructive EVT for ruptured fusiform aneurysms. Our findings suggest that clinical outcome may be more dependent on initial H/H grade and not necessarily the type of endovascular procedure performed.
There are some limitations to consider when interpreting the results of the current study. First, the sample size was not sufficient to warrant statistical exploration of predictors of clinical response by regression analysis. Second, most patients in this study undergoing emergency EVT of ruptured aneurysms were lost to follow-up after their initial hospital course. Limited data regarding long-term angiographic and clinical follow-up data, especially for those patients in the SAH group, precluded statistical analysis of long-term stability of EVT and clinical outcome. Finally, the current study did not evaluate the use of flow-diverting devices as a method of reconstructive EVT. This new technology appears promising, given its theoretical advantage in providing a more physiologic and durable treatment of fusiform intracranial aneurysms compared with existing reconstructive methods. While initial studies are promising, the long-term safety and clinical efficacy of such devices are unknown.11–13
Conclusion
Despite the aforementioned limitations, this study differs from previous retrospective analyses of intracranial fusiform aneurysms in that most of the patients undergoing reconstructive EVT presented with SAH. This study suggests that, in this group of patients, reconstructive EVT may be associated with a higher incidence of intraprocedural complications and poor clinical outcomes; however, given the small sample size of patients with ruptured aneurysms undergoing reconstructive EVT, definitive conclusions cannot be inferred. Future studies with larger sample sizes are needed to investigate the predictors of clinical outcome in patients undergoing reconstructive EVT for ruptured intracranial fusiform aneurysms.
References
Footnotes
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Competing interests None.
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Ethics approval Institutional Review Board approval was obtained for this study.
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Provenance and peer review Not commissioned; externally peer reviewed.