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Giuseppe Lanzino and David F. Kallmes

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Ross C. Puffer, David F. Kallmes, Harry J. Cloft and Giuseppe Lanzino

Object

In this study the authors determined the patency rate of the ophthalmic artery (OphA) after placement of 1 or more flow diversion devices across the arterial inlet for treatment of proximal internal carotid artery (ICA) aneurysms, and correlated possible risk factors for OphA occlusion.

Methods

Nineteen consecutive patients were identified (mean age 53.9 years, range 23–74 years, all female) who were treated for 20 ICA aneurysms. In all patients a Pipeline Embolization Device (PED) was placed across the ostium of the OphA while treating the target aneurysm. Flow through the OphA after PED placement was determined by immediate angiography as well as follow-up angiograms (mean 8.7 months), compared with the baseline study. Potential risk factors for OphA occlusion, including age, immediate angiographic flow through the ophthalmic branch, status of flow within the aneurysm after placement of PEDs, whether the ophthalmic branch originated from the aneurysm dome, and number of PEDs placed across the ophthalmic branch inlet were correlated with patency rate.

Results

Patients were treated with 1–3 PEDs (3 aneurysms treated with placement of 1 PED, 12 with 2 PEDs, and 5 with 3 PEDs). In 17 (85%) of 20 treated aneurysms, no changes in the OphA flow were noted immediately after placement of the device. Two (10%) of 20 patients had delayed antegrade filling immediately following PED placement and 1 patient (5%) had retrograde flow from collaterals to the OphA immediately after placement of the device. One patient (5%) experienced delayed asymptomatic ICA occlusion; this patient was excluded from analysis at follow-up. At follow-up the OphA remained patent with normal antegrade flow in 13 (68%) of 19 patients, patent but with slow antegrade flow in 2 patients (11%), and was occluded in 4 patients (21%). No visual changes or clinical symptoms developed in patients with OphA flow compromise. The mean number of PEDs in the patients with occluded OphAs or change in flow at angiographic follow-up was 2.4 (SEM 0.2) compared with 1.9 (SEM 0.18) in the patients with no change in OphA flow (p = 0.09). There was no significant difference between the patients with occluded OphAs compared with nonoccluded branches based on patient age, immediate angiographic flow through the ophthalmic branch, status of flow through the aneurysm after placement of PEDs, whether the ophthalmic branch originated from the aneurysm dome, or number of PEDs placed across the ophthalmic branch inlet.

Conclusions

Approximately one-quarter of OphAs will undergo proximal thrombosis when covered with flow diversion devices. Even though these events were well-tolerated clinically, our findings suggest that coverage of branch arteries that have adequate collateral circulation may lead to spontaneous occlusion of those branches.

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Waleed Brinjikji, David F. Kallmes, Harry J. Cloft and Giuseppe Lanzino

OBJECT

The association between age and outcomes following aneurysm treatment with flow diverters such as the Pipeline Embolization Device (PED) have not been well established. Using the International Retrospective Study of the Pipeline Embolization Device (IntrePED) registry, the authors assessed the age-related clinical outcomes of patients undergoing aneurysm embolization with the PED.

METHODS

Patients with unruptured aneurysms in the IntrePED registry were divided into 4 age groups: ≤ 50, 51–60, 61–70, and > 70 years old. The rates of the following postoperative complications were compared between age groups using chi-square tests: spontaneous rupture, intracranial hemorrhage (ICH), ischemic stroke, parent artery stenosis, cranial neuropathy, neurological morbidity, neurological mortality, combined neurological morbidity and mortality, and all-cause mortality. The association between age and these complications was tested in a multivariate logistic regression analysis adjusted for sex, number of PEDs, and aneurysm size, location, and type.

RESULTS

Seven hundred eleven patients with 820 unruptured aneurysms were included in this study. Univariate analysis demonstrated no significant difference in ICH rates across age groups (lowest 1.0% for patients ≤ 50 years old and highest 5.0% for patients > 70 years old, p = 0.097). There was no difference in ischemic stroke rates (lowest 3.6% for patients ≤ 50 years old and highest 6.0% for patients 50–60 years old, p = 0.73). Age > 70 years old was associated with higher rates of neurological mortality; patients > 70 years old had neurological mortality rates of 7.4% compared with 3.3% for patients 61–70 years old, 2.7% for patients 51–60 years old, and 0.5% for patients ≤ 50 years old (p = 0.006). On multivariate logistic regression analysis, increasing age was associated with higher odds of combined neurological morbidity and mortality (odds ratio 1.02, 95% confidence interval 1.00–1.05; p = 0.03).

CONCLUSIONS

Increasing age is associated with higher neurological morbidity and mortality after Pipeline embolization of intracranial aneurysms. However, the overall complication rates of PED treatment in this group of highly selected elderly patients (> 70 years) were acceptably low, suggesting that age alone should not be considered an exclusion criterion when considering treatment of intracranial aneurysms with the PED.

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Ross C. Puffer, David J. Daniels, David F. Kallmes, Harry J. Cloft and Giuseppe Lanzino

Object

The authors conducted a study to review their experience with tentorial dural arteriovenous fistulas (DAVFs) treated with transarterial endovascular embolization in which Onyx was used.

Methods

The authors reviewed prospectively collected data in 9 patients with tentorial DAVFs treated with Onyx embolization between 2008 and 2011. Information reviewed included clinical presentation, angiographic features, treatment, and clinical and radiologically documented outcome. Clinical follow-up was available in every patient. Radiological follow-up studies were available in 8 of 9 patients (mean follow-up 4.6 months).

Results

Six of 9 patients had complete angiographic obliteration (in 5 this was confirmed by a follow-up angiogram obtained 3–6 months later), and 2 patients had near-complete obliteration (faint filling of the venous drainage in the late venous phase). One patient had partial obliteration and required surgical disconnection. In all patients with complete obliteration, transarterial embolization was performed through the posterior branch of the middle meningeal artery. There were no procedural complications, and no morbidity or mortality resulted from Onyx embolization.

Conclusions

Transarterial Onyx embolization is a valid, effective, and safe alternative to surgical disconnection in many patients with tentorial DAVFs. The presence of an adequate posterior branch of the middle meningeal artery is critical to achieve a microcatheter position distal enough to increase the likelihood of complete obliteration.

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Ioannis Loumiotis, Robert D. Brown Jr., Roanna Vine, Harry J. Cloft, David F. Kallmes and Giuseppe Lanzino

Object

The management of incidental small unruptured intracranial aneurysms (UIAs) is controversial and many factors need to be considered in the decision-making process. The authors describe a large consecutive series of patients harboring small incidental intracranial aneurysms. Treatment strategy, natural history, complications, and short-term outcomes are presented.

Methods

Between January 2008 and May 2011, the authors prospectively evaluated 212 patients with 272 small (< 10-mm) incidental aneurysms. Treatment recommendations (observation, endovascular treatment, or surgery), complications of treatment, and short-term outcomes were assessed.

Results

Recommended treatment consisted of observation in 125 patients, endovascular embolization in 64, and surgery in 18. Six patients were excluded from further analysis because they underwent treatment elsewhere. In the observation group, at a mean follow-up of 16.7 months, only 1 patient was moved to the embolization group. Seven (6%) of the 125 patients in the observation group died of causes unrelated to aneurysm. Sixty-five patients underwent 69 embolization procedures. The periprocedural permanent morbidity and mortality rates in patients undergoing endovascular treatment were 1.5% and 1.5%, respectively (overall morbidity and mortality rate 3.0%). In the surgery group no periprocedural complications were observed, although 1 patient did not return to her previous occupation. No aneurysmal rupture was documented in any of the 3 treatment groups during the follow-up period.

Conclusions

A cautious and individualized approach to incidental UIAs is of utmost importance for formulation of a safe and effective treatment algorithm. Invasive treatment (either endovascular or surgery) can be considered in selected younger patients, certain “higher-risk” locations, expanding aneurysms, patients with a family history of aneurysmal hemorrhage, and in those who cannot live their lives knowing that they harbor the UIA. Although the complication rate of invasive treatment is very low, it is not negligible. The study confirms that small incidental UIAs deemed to be not in need of treatment have a very benign short-term natural history, which makes observation a reasonable approach in selected patients.

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Vance T. Lehman, Waleed Brinjikji, Mahmud Mossa-Basha, Giuseppe Lanzino, Alejandro A. Rabinstein, David F. Kallmes and John Huston III

Intracranial aneurysms are heterogeneous in histopathology and imaging appearance. The biological behavior of different types of aneurysms is now known to depend on the structure and physiology of the aneurysm wall itself in addition to intraluminal flow and other luminal features. Aneurysm wall structure and imaging markers of physiology such as aneurysm wall enhancement have been assessed in many prior investigations using conventional-resolution MRI. Recently, high-resolution vessel wall imaging (HR-VWI) techniques with MRI have been introduced. Reports of findings on high-resolution imaging have already emerged for many types of aneurysms demonstrating detailed characterization of wall enhancement, thickness, and components, but many questions remain unexplored. This review discusses the key HR-VWI literature to date. Aneurysm wall findings on conventional-resolution MRI are also discussed as these may help one understand the potential utility and findings on HR-VWI for various aneurysm types. The authors have illustrated these points with several examples demonstrating both features already described in the literature and novel cases demonstrating the potential for future clinical and research applications.

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Waleed Brinjikji, Ravi K. Lingineni, Chris N. Gu, Giuseppe Lanzino, Harry J. Cloft, Lauren Ulsh, Kristen Koeller and David F. Kallmes

OBJECT

Tobacco smoking is one of the most important risk factors for the formation of intracranial aneurysms and for aneurysmal subarachnoid hemorrhages. Smoking has also been suggested to contribute to the recurrence of aneurysms after endovascular coiling. To improve the understanding of the impact of smoking on long-term outcomes after coil embolization of intracranial aneurysms, the authors studied a consecutive contemporary series of patients treated at their institution. The aims of this study were to determine whether smoking is an independent risk factor for aneurysm recurrence and retreatment after endovascular coiling.

METHODS

All patients who had received an intrasaccular coil embolization of an intracranial aneurysm, who had undergone a follow-up imaging exam at least 6 months later, and whose smoking history had been recorded from January 2005 through December 2012 were included in this study. Patients were stratified according to smoking status into 3 groups: 1) never a smoker, 2) current smoker (smoked at the time of treatment), and 3) former smoker (quit smoking before treatment). The 2 primary outcomes studied were aneurysm recurrence and aneurysm retreatment after treatment for endovascular aneurysms. Kruskal-Wallis and chi-square tests were used to test statistical significance of differences in the rates of aneurysm recurrence, retreatment, or of both among the 3 groups. A multivariate logistic regression analysis controlling for smoking status and for several characteristics of the aneurysm was also performed.

RESULTS

In total, 384 patients with a combined total of 411 aneurysms were included in this study. The aneurysm recurrence rate was not significantly associated with smoking: both former smokers (OR 1.00, 95% CI 0.61–1.65; p = 0.99) and current smokers (OR 0.58, 95% CI 0.31–1.09; p = 0.09) had odds of recurrence that were similar to those who were never smokers. Former smokers (OR 0.78, 95% CI 0.46–1.35; p = 0.38) had odds of retreatment similar to those of never smokers, and current smokers had a lower odds of undergoing retreatment (OR 0.44, 95% CI 0.21–0.91; p = 0.03) than never smokers. Moreover, an analysis adjusting for aneurysm rupture, diameter, and initial occlusion showed that former smokers (OR 0.65, 95% CI 0.33–1.28; p = 0.21) and current smokers (OR 1.04, 95% CI 0.60–1.81; p = 0.88) had odds of aneurysm recurrence similar to those who were never smokers. Adjusting the analysis for aneurysm rupture, diameter, and occlusion showed that both former smokers (OR 0.49, 95% CI 0.23–1.05; p = 0.07) and current smokers (OR 0.82, 95% CI 0.46–1.46; p = 0.50) had odds of retreatment similar to those of patients who were never smokers.

CONCLUSIONS

The results show that smoking was not an independent risk factor for aneurysm recurrence and aneurysm retreatment among patients receiving endovascular treatment for intracranial aneurysms at the authors' institution. Nonetheless, patients with intracranial aneurysms should continue to be counseled about the risks of tobacco smoking.

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Waleed Brinjikji, Mariangela Piano, Shanna Fang, Guglielmo Pero, David F. Kallmes, Luca Quilici, Luca Valvassori, Emilio Lozupone, Harry J. Cloft, Edoardo Boccardi and Giuseppe Lanzino

OBJECT

Flow-diversion treatment has been shown to be associated with high rates of angiographic obliteration; however, the treatment is relatively contraindicated in the acute phase following subarachnoid hemorrhage (SAH) as these patients require periprocedural dual antiplatelet therapy. Acute coiling followed by flow diversion has emerged as an intriguing and feasible treatment option for ruptured complex and giant aneurysms. In this study the authors report outcomes and complications of patients with ruptured aneurysms undergoing coiling in the acute phase followed by planned delayed flow diversion.

METHODS

This case series includes patients from 2 institutions. All patients underwent standard endovascular coiling in the acute phase after SAH with the intention and plan to proceed with flow diversion at a later date. Outcomes studied included angiographic occlusion, procedure-related complications, and long-term clinical outcome as measured using the modified Rankin Scale.

RESULTS

A total of 31 patients underwent coiling in the acute phase with the intention to undergo flow diversion at a later date. The mean aneurysm size was 15.8 ± 7.9 mm. Of the 31 patients undergoing coiling, 4 patients could not undergo further flow-diverter therapy: 3 patients (9.7%) died of complications of subarachnoid hemorrhage and 1 patient had permanent morbidity as a result of perioperative ischemic stroke (3.1%). Twenty-seven patients underwent staged placement of flow diverters after adequate recovery. The median time to treatment was 16 weeks. There was one case of aneurysm rebleeding following coil treatment. There were no cases of permanent morbidity or mortality resulting from flow-diverter treatment. Twenty-four patients underwent imaging follow-up; 18 of these patients had aneurysms that were completely or nearly completely occluded (58.1% on an intent-to-treat basis). At last follow-up (mean 18.3 months), 25 patients had mRS scores ≤ 2 (80.6% on an intent-to-treat basis).

CONCLUSIONS

Staged treatment of ruptured complex and giant intracranial aneurysms with coiling in the acute phase and flow-diverter treatment following recovery from SAH is both safe and effective. In this series, no cases of rebleeding occurred during the interval between coiling and flow diversion. This strategy should be considered as a valid option in patients presenting with these challenging ruptured aneurysms.

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Daniel H. Sahlein, Mohammad Fouladvand, Tibor Becske, Isil Saatci, Cameron G. McDougall, István Szikora, Giuseppe Lanzino, Christopher J. Moran, Henry H. Woo, Demetrius K. Lopes, Aaron L. Berez, Daniel J. Cher, Adnan H. Siddiqui, Elad I. Levy, Felipe C. Albuquerque, David J. Fiorella, Zsolt Berentei, Miklos Marosfoi, Saruhan H. Cekirge, David F. Kallmes and Peter K. Nelson

OBJECT

Neuroophthalmological morbidity is commonly associated with large and giant cavernous and supraclinoid internal carotid artery (ICA) aneurysms. The authors sought to evaluate the neuroophthalmological outcomes after treatment of these aneurysms with the Pipeline Embolization Device (PED).

METHODS

The Pipeline for Uncoilable or Failed Aneurysms (PUFS) trial was an international, multicenter prospective trial evaluating the safety and efficacy of the PED. All patients underwent complete neuroophthalmological examinations both before the PED procedure and at a 6-month follow-up. All examinations were performed for the purpose of this study and according to study criteria.

RESULTS

In total, 108 patients were treated in the PUFS trial, 98 of whom had complete neuroophthalmological follow-up. Of the patients with complete follow-up, 39 (40%) presented with a neuroophthalmological baseline deficit that was presumed to be attributable to the aneurysm, and patients with these baseline deficits had significantly larger aneurysms. In 25 of these patients (64%), the baseline deficit showed at least some improvement 6 months after PED treatment, whereas in 1 patient (2.6%), the deficits only worsened. In 5 patients (5%), new deficits had developed at the 6-month follow-up, while in another 6 patients (6%), deficits that were not originally assumed to be related to the aneurysm had improved by that time. A history of diabetes was associated with failure of the baseline deficits to improve after the treatment. The aneurysm maximum diameter was significantly larger in patients with a new deficit or a worse baseline deficit at 6 months postprocedure.

CONCLUSIONS

Patients treated with the PED for large and giant ICA aneurysms had excellent neuroophthalmological outcomes 6 months after the procedure, with deficits improving in most of the patients, very few deficits worsening, and few new deficits developing.

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Tibor Becske, Matthew B. Potts, Maksim Shapiro, David F. Kallmes, Waleed Brinjikji, Isil Saatci, Cameron G. McDougall, István Szikora, Giuseppe Lanzino, Christopher J. Moran, Henry H. Woo, Demetrius K. Lopes, Aaron L. Berez, Daniel J. Cher, Adnan H. Siddiqui, Elad I. Levy, Felipe C. Albuquerque, David J. Fiorella, Zsolt Berentei, Miklós Marosföi, Saruhan H. Cekirge and Peter K. Nelson

OBJECTIVE

The long-term effectiveness of endovascular treatment of large and giant wide-neck aneurysms using traditional endovascular techniques has been disappointing, with high recanalization and re-treatment rates. Flow diversion with the Pipeline Embolization Device (PED) has been recently used as a stand-alone therapy for complex aneurysms, showing significant improvement in effectiveness while demonstrating a similar safety profile to stent-supported coil treatment. However, relatively little is known about its long-term safety and effectiveness. Here the authors report on the 3-year safety and effectiveness of flow diversion with the PED in a prospective cohort of patients with large and giant internal carotid artery aneurysms enrolled in the Pipeline for Uncoilable or Failed Aneurysms (PUFS) trial.

METHODS

The PUFS trial is a prospective study of 107 patients with 109 aneurysms treated with the PED. Primary effectiveness and safety end points were demonstrated based on independently monitored 180-day clinical and angiographic data. Patients were enrolled in a long-term follow-up protocol including 1-, 3-, and 5-year clinical and imaging follow-up. In this paper, the authors report the midstudy (3-year) effectiveness and safety data.

RESULTS

At 3 years posttreatment, 74 subjects with 76 aneurysms underwent catheter angiography as required per protocol. Overall, complete angiographic aneurysm occlusion was observed in 71 of these 76 aneurysms (93.4% cure rate). Five aneurysms were re-treated, using either coils or additional PEDs, for failure to occlude, and 3 of these 5 were cured by the 3-year follow-up. Angiographic cure with one or two treatments of Pipeline embolization alone was therefore achieved in 92.1%. No recanalization of a previously completely occluded aneurysm was noted on the 3-year angiograms. There were 3 (2.6%) delayed device- or aneurysm-related serious adverse events, none of which led to permanent neurological sequelae. No major or minor late-onset hemorrhagic or ischemic cerebrovascular events or neurological deaths were observed in the 6-month through 3-year posttreatment period. Among 103 surviving patients, 85 underwent functional outcome assessment in which modified Rankin Scale scores of 0–1 were demonstrated in 80 subjects.

CONCLUSIONS

Pipeline embolization is safe and effective in the treatment of complex large and giant aneurysms of the intracranial internal carotid artery. Unlike more traditional endovascular treatments, flow diversion results in progressive vascular remodeling that leads to complete aneurysm obliteration over longer-term follow-up without delayed aneurysm recanalization and/or growth.

Clinical trial registration no.: NCT00777088 (clinicaltrials.gov)