Abstract
Purpose
Flow diverting stents have revolutionized the treatment of intracranial aneurysms through endoluminal reconstruction of the parent vessel. Despite this, certain aneurysms require retreatment. The purpose of this study was to identify clinical and radiologic determinants of aneurysm retreatment following flow diversion.
Methods
A multicenter flow diversion database was evaluated to identify patients presenting with an unruptured, previously untreated aneurysm with a minimum of 12 months’ clinical and angiographic follow-up. Univariate and multivariate logistic regression modeling was performed to identify determinants of retreatment.
Results
We identified 189 aneurysms treated in 189 patients with a single flow-diverting stent. Mean age was 54 years, and 89% were female. Complete occlusion was achieved in 70.3% and 83.6% of patients at six and 12 months, respectively. Aneurysm retreatment with additional flow-diverting stents occurred in 5.8% of cases. Univariate analysis revealed that dome diameter 10 mm (p = 0.012), pre-clinoid internal carotid artery location (p = 0.012), distal > proximal parent vessel diameter (p = 0.042), and later dual antiplatelet therapy (DAPT) discontinuation (p < 0.001) were predictive of retreatment. Multivariate analysis identified discontinuation of DAPT 12 months (p = 0.003) as a strong determinant of retreatment with dome diameter 10 mm trending toward statistical significance (p = 0.064). Large aneurysm neck diameter, presence of aneurysm branch vessels, patient age, smoking history, and hypertension were not determinant of retreatment on multivariate analysis.
Conclusions
Prolonged DAPT is the most important determinant of aneurysm retreatment following single-device flow diversion. Abbreviating DAPT duration to only six months should be a consideration in this population, especially for patients with a large aneurysm dome diameter.
Keywords: Aneurysm, endovascular, flow diversion, retreatment
Introduction
Endoluminal flow diversion is an endovascular technique that promotes intrasaccular thrombosis and neointimal growth across the neck of an intracranial aneurysm, excluding it from the intracranial circulation. 1 The Pipeline Embolization Device (PED; Medtronic, Minneapolis, MN, USA) was the first such stent in widespread clinical use, designed for the treatment of large aneurysms of the internal carotid artery. Initially deployed as multiple overlapping devices, practice has shifted to utilizing a single device for most patients. 2
Despite an increasing body of evidence supporting the clinical safety and efficacy of the PED for the treatment of aneurysms,3,4 some aneurysms do not completely occlude, requiring additional delayed treatment. Although multiple investigations have been performed evaluating determinants of aneurysm non-occlusion following PED placement, there is a paucity of published data evaluating determinants of aneurysm retreatment, which may be distinct from determinants of non-occlusion. The purpose of this large, multicenter, retrospective cohort study is to assess outcomes after PED treatment with the specific goal of identifying clinical and radiologic determinants of aneurysm retreatment following deployment of a single PED in diverse clinical practice settings.
Methods
Study population
The study was approved by the local institutional review boards at participating centers. Informed consent was waived based on minimal patient risk and practical inability to perform the study without the waiver. A retrospective analysis was performed on a large, prospectively maintained, multicenter aneurysm database of patients treated with PED flow diversion. To be included in the final analysis, patients had to be 18 years old, possess an unruptured intracranial aneurysm that had not been previously treated, have only a single PED without adjunct coiling placed at the time of intervention for treatment of a single aneurysm, and have 12-months of angiographic and clinical follow-up. A total of 300 patients underwent single PED placement for the treatment of intracranial aneurysms at four participating US tertiary care centers (52 patients at University of Texas Health Science Center at San Antonio, San Antonio, TX; 127 patients at Massachusetts General Hospital, Boston, MA; 61 patients at University of Colorado, Aurora, CO; 60 patients at Westchester Medical Center, Valhalla, NY) between 1 December 2012 and 15 January 2020. One hundred and eleven patients were subsequently excluded, leaving 189 patients who received single PED flow-diversion for the treatment of 189 intracranial aneurysms in the final study cohort (Figure 1).
Figure 1.
Patient recruitment and cohort development.
PED: Pipeline Embolization Device.
Treatment description
Management decisions were at the discretion of treating neurointerventionalists. In all cases, surgical and alternative endovascular interventions were considered. Aneurysms involving the distal anterior circulation (i.e. the anterior and middle cerebral arteries) or posterior circulation were eligible for “off-label” PED treatment. Local operating procedures were followed at each clinical site. Antiplatelet regimens before and after intervention were prescribed according to the local practice preferences with continuation or cessation of dual antiplatelet therapy (DAPT) commonly decided at six-month angiographic follow-up. PEDs were deployed through a 0.027-inch diameter microcatheter (Marksman: ev3/Covidien, Dublin, Ireland; Phenom: Medtronic, Minneapolis, MN, USA). The size of the PED used was at the discretion of each treating neurointerventionalist. Transfemoral arterial access was acquired in all cases. The timing of angiographic follow-up was also neurointerventionalist-dependent but typically consisted of catheter angiography performed at six, 12, and 18–24 months. Angiographic outcome was self-reported. Retreatment with additional PEDs was ultimately decided by the treating neurointerventionalist and was typically due to persistent filling of the aneurysm dome.
Clinical data and outcomes
All aneurysms were assessed for occlusion on follow-up angiographic imaging. If angiography demonstrated residual opacification of the aneurysm (neck and/or dome), the aneurysm was categorized as non-occluded. Intracranial or access site adverse events occurring within 90 days of PED placement were classified as intervention-related complications. Major complications included death, intracranial hemorrhage (ICH), ischemic stroke, or retroperitoneal hematoma. Minor complications included transient ischemic attack (TIA), cranial neuropathy, and groin hematoma.
Pertinent patient demographic and clinical data was collected from the medical record. Aneurysm morphologic characteristics were collected from patient-specific catheter angiograms. The antiplatelet agents used and timing of initiation and discontinuation of DAPT were collected for each patient with early discontinuation of DAPT defined as occurring ≤12 months following PED placement and delayed discontinuation of DAPT defined as occurring >12 months following PED placement.
Statistical analysis
Means, standard deviations, frequencies, or percentages were used for descriptive statistics. Comparisons between continuous variables were performed using a two-tailed t-test. Proportions were compared using the Fisher exact or Chi-square tests. Univariate analysis was used to identify variables with p < 0.05 for inclusion in our multivariate logistic regression model. Multivariate logistic regression modeling was subsequently performed to identify variables determinant for retreatment. A p-value < 0.05 was denoted to be statistically significant. All statistical analyses were performed using SPSS software (version 22.0; IBM Corporation, Armonk, NY, USA).
Results
Cohort characterization
A total of 189 intracranial aneurysms were treated with single PED flow-diversion in 189 patients with an average follow-up time of 12.4 ± 2.5 months and were subsequently included in the final study cohort. The mean age of included patients was 54 years; 89% of the cohort was female. Small aneurysms (maximum dome diameter <10 mm) accounted for 85% of the aneurysms treated. The average aneurysm dome diameter was 6.5 ± 4.0 mm with an average neck diameter of 4.0 ± 1.7 mm. Nearly 44% of treated aneurysms involved a branch vessel with 54.9% of branch vessels arising from the parent vessel immediately adjacent to the aneurysm neck, 30.5% from the aneurysm neck, and 14.6% from the aneurysm dome. The distribution of aneurysms within the intracranial circulation is detailed in Table 1, with 98.4% of aneurysms involving the anterior circulation.
Table 1.
Cohort demographics and aneurysm morphology.
| Characteristics | Single treatment (%) | Retreatment (%) | p-value |
|---|---|---|---|
| Total cases | 178 (94.2) | 11 (5.8) | – |
| Average age, years | 54.0 ± 12.6 | 59.6 ± 10.5 | 0.158 |
| Female sex | 159 (89.3) | 10 (90.1) | 0.868 |
| Mean aneurysm size, mm | 6.4 ± 3.8 | 8.3 ± 5.9 | 0.012 |
| Small, <10 mm | 155 (87.1) | 6 (54.5) | |
| Large, ≥10 mm | 23 (12.9) | 5 (45.5) | |
| Mean neck diameter, mm | 4.0 ± 1.7 | 4.5 ± 1.4 | 0.322 |
| Vessel segment | 0.012 | ||
| Cavernous ICA | 19 | 1 | |
| Clinoid ICA | 4 | 0 | |
| Ophthalmic ICA | 114 | 5 | |
| Communicating ICA | 18 | 3 | |
| NOS ICA | 6 | 0 | |
| Distal anterior circulation | 15 | 1 | |
| Posterior circulation | 2 | 1 | |
| Branch vessel present | 75 (42.1) | 8 (72.7) | |
| Parent vessel | 44 (58.6) | 2 (25.0) | |
| Neck | 20 (26.7) | 5 (62.5) | 0.062 |
| Dome | 11 (14.7) | 1 (12.5) | |
| Max parent vessel diameter at aneurysm neck, mm | 3.6 ± 0.7 | 3.3 ± 0.7 | 0.368 |
| Max parent vessel diameter distal to aneurysm, mm | 3.5 ± 0.6 | 3.4 ± 0.9 | 0.042 |
| ΔDa, mm | 0.42 ± 0.59 | 0.43 ± 0.56 | 0.499 |
| Mean length of DAPT, months | 7.1 ± 3.1 | 15.0 ± 11.2 | <0.001 |
aΔD = Pipeline Embolization Device diameter – maximum parent vessel diameter at aneurysm neck.
ICA: internal carotid artery; NOS: not otherwise specified; DAPT: dual antiplatelet therapy.
The mean parent vessel diameter measured at the aneurysm neck was 3.6 ± 0.8 mm. The average PED diameter used was 4.0 ± 0.7 mm (2.5–5.0 mm) with an average length of 15.7 ± 4.6 mm (10–39 mm). The average difference between the PED diameter and the parent vessel diameter measured at the aneurysm neck (ΔD) was 0.4 ± 0.6 mm (–1.6 to 2.66 mm). Following PED placement, patients were placed on DAPT for an average of 7.4 ± 3.8 months (duration range: 3–30 months). Most patients received a combination of clopidogrel and aspirin (72.5%) with a minority receiving prasugrel and aspirin (16.4%), ticagrelor and aspirin (10.6%), or clopidogrel and ticagrelor (0.5%). A total of 11 (5.8%) patients required aneurysm retreatment with placement of additional PED flow-diverters due to residual aneurysm dome filling (Table 1).
PED treatment outcomes
Complications occurred in 7.4% of cases. Major complications were identified in 4.2%, including ICH in 2.6%, ischemic stroke in 1.1%, and retroperitoneal hematoma in 0.5% of cases. The single episode of retroperitoneal hematoma was managed non-operatively. Both episodes of ischemic stroke occurred within 90 days of PED placement with one episode occurring in a patient with normal (≤6 months) discontinuation of DAPT and one episode occurring in a patient with late (>12 months) discontinuation of DAPT. No procedure-related deaths were observed. Minor complications were identified in 3.2%, including TIA in 2.1%, cranial neuropathies in 0.5%, and groin hematomas in 0.5% of cases (Table 2).
Table 2.
Total aneurysm non-occlusion rates and adverse events.
| Non-occlusion rates | Count (%) | ||
|---|---|---|---|
| Six months | 55 (29.1) | ||
| 12 months | 31 (16.4) | ||
| >12 months | 26 (13.8) | ||
| Total adverse events | Count (%) | ||
| Major complications | 8 (4.2) | ||
| Death | 0 | ||
| ICH | 5 (2.6) | ||
| Ischemic stroke | 2 (1.1) | ||
| Retroperitoneal hemorrhage | 1 (0.5) | ||
| Minor complications | 6 (3.2) | ||
| TIA | 4 (2.1) | ||
| Cranial neuropathy | 1 (0.5) | ||
| Groin hematoma | 1 (0.5) |
ICH: intracranial hemorrhage; TIA: transient ischemic attack.
Residual aneurysm neck and/or dome opacification was observed in 29.1% and 16.4% of all patients at six and 12 months post-procedure, respectively. Residual aneurysm filling persisted in 13.8% of treated aneurysms on angiographic follow-up performed more than 12 months after flow-diversion (Table 2). A total of 11 (5.8%) patients required retreatment with placement of one or more PED flow diverters for residual dome filling. All retreatments were performed ≥12 months after initial intervention with four (36.4%) performed >18 months after initial intervention. Angiographic follow-up was available on five patients following retreatment. Of these individuals, all five (100%) demonstrated complete aneurysm occlusion on follow-up angiography (Figure 2). No major complications were reported in the retreatment group, with one (9.1%) patient experiencing a TIA that resolved without additional intervention.
Figure 2.
(a) and (b) 3D and Anteroposterior (AP) projection Digital Subtraction Angiography (DSA) images demonstrating a right M1 aneurysm (white arrow) with perforator lenticulostriate arteries arising from the aneurysm dome (black arrows). (c) Twelve-month follow-up after single Pipeline Embolization Device (PED) placement with residual filling of the dome. (d) Six-month follow-up after placement of second PED now with obliteration of the aneurysm sac (white asterisk) and preserved perforator flow (black arrows).
Determinants of retreatment
All 189 patients had angiographic follow-up performed at least 12 months after PED placement; 170 patients had angiographic follow-up performed at exactly 12 months. Univariate analysis of radiologic variables revealed that a maximum aneurysm dome diameter ≥10 mm (p = 0.012), distal > proximal parent vessel diameter (p = 0.042), and pre-clinoid internal carotid artery (ICA) segment involvement (vs. post-clinoid segment; p = 0.012) were determinants of aneurysm retreatment. Univariate analysis of clinical variables demonstrated that the DAPT discontinuation >12 months (p < 0.001) was a determinant of retreatment whereas patient age, smoking history, hypertension, and family history of intracranial aneurysms were not (Table 3).
Table 3.
Multivariate logistic regression modeling determinants of aneurysm retreatment.
| Predictor | Adjusted odds ratio | 95% confidence interval | p-value |
|---|---|---|---|
| Aneurysm size (<10 mm vs. ≥10 mm) | 10.49 | 0.87–126.64 | 0.064 |
| Parent vessel diameter distal to aneurysm | 3.65 | 0.56–24.00 | 0.177 |
| Vessel segment (pre- vs. post-clinoid segments) | 10.72 | 0.68–169.45 | 0.092 |
| Length of DAPT | 1.24 | 1.08–1.43 | 0.003 |
DAPT: dual antiplatelet therapy.
Prolonged use of DAPT with discontinuation >12 months after PED placement was the only variable to remain a statistically significant determinant of retreatment on multivariate analysis (odds ratio (OR) 1.24, 95% confidence interval (CI) 1.08–1.43, p = 0.003; Table 3). Aneurysm dome diameter did not reach statistical significance as a determinant of retreatment on multivariate analysis (p = 0.064). Notable variables that were tested but were not associated with aneurysm retreatment included aneurysm neck diameter, branch vessel inclusion within the aneurysm, the size of the parent artery at the aneurysm neck, and the difference between the parent artery diameter and PED diameter (ΔD).
Discussion
In the current study, we identified determinants of aneurysm retreatment following flow diversion with a single PED. Univariate analysis revealed that a large aneurysm dome diameter (≥10 mm), a distal > proximal parent vessel diameter, aneurysmal involvement of pre-clinoid ICA segments, and prolonged use of DAPT were statistically significant determinants of aneurysm retreatment. Multivariate analysis demonstrated that only prolonged use of DAPT for more than 12 months remained a statistically significant determinant of retreatment with a large aneurysm dome diameter trending towards, but not reaching, statistical significance. Interestingly, morphologic features of the aneurysm and parent vessel and clinical factors such as age, smoking history, and hypertension were not associated with future retreatment.
The current study demonstrated six- and 12-month occlusion rates of 70.9% and 83.6%, respectively, with a retreatment rate of 5.8%, which agrees with results published elsewhere. Specifically, the prospective Pipeline for Uncoilable or Failed Aneurysms Trial demonstrated complete aneurysm occlusion in over 70% of cases treated with PED at 180 days follow-up 5 with a long-term occlusion rate of 86.8% at one-year follow-up and a retreatment rate less than 6%. 6 PED-associated morbidity and mortality rates were also low in the current study, with major neurologic complications occurring in 4.2% of cases with procedure-related stroke and ICH occurring in 1.1% and 2.6% of all cases, respectively. In comparison, PED-related morbidity and mortality have been reported at 5.8% and 2.2% in the published literature, respectively, with ischemic stroke occurring in up to 3% of cases and intracranial hemorrhage occurring in 2.7% of cases. 7
Although morphologic variables have been associated with aneurysm non-occlusion, little work has been done to identify the pertinent morphologic and clinical factors determinant of aneurysm retreatment. Specifically, we hypothesized that the decision to retreat aneurysms following flow-diversion was influenced by a combination of patient-specific morphologic and clinical factors in addition to the extent of residual aneurysm filling on angiographic follow-up. Prolonged use of DAPT for more than 12 months following PED placement was independently associated with aneurysm retreatment in our study cohort with the variability in length of DAPT post flow diversion potentially reflecting a lack of clear, evidence-based guidance on the optimal timing for DAPT discontinuation.8–12 In a meta-analysis performed by Texakalidis and colleagues in which both procedure-related complications and the DAPT regimen used following PED placement were evaluated, the authors reported that over 90% of treated patients received a combination of aspirin and clopidogrel for 3–12 months following PED placement. 13 This large variability in the duration of DAPT used in clinical practice is further supported by work performed by Gupta and colleagues, in which the practice habits of neurointerventionalists in 15 states were evaluated using objective questionnaire data. The authors reported that over 46% of respondents routinely kept patients on DAPT for more than seven months following PED placements whereas roughly 42% of respondents maintained patients on DAPT for 2–6 months. 14 The impact DAPT has on aneurysm occlusion following PED placement has not been well-evaluated in the published literature. Platz et al. evaluated the long-term effects of antiplatelet therapy on aneurysm occlusion following endovascular coiling. Although aneurysm recanalization was not influenced by the administration of aspirin alone, recanalization occurred significantly more frequently in patients treated with DAPT (p = 0.028). Interestingly, antiplatelet medications (including DAPT) did not increase the risk of a second endovascular intervention. 15 Given the paucity of published data evaluating the effect of DAPT on aneurysm non-occlusion rates following flow diversion, further investigation is warranted to further discern the optimal timing of DAPT discontinuation.
Large aneurysm dome diameter (⩾10 mm) was associated with aneurysm retreatment on univariate analysis in the current study cohort, but the statistical significance of this finding did not persist on multivariate logistic regression modeling. Rather, this morphologic variable demonstrated a trend toward statistical significance (OR 10.49, 95% CI 0.87–126.64, p = 0.064), potentially reflecting an insufficient cohort sample size to detect statistical significance for this variable. Large dome diameter has been identified as a risk factor for aneurysm non-occlusion following PED placement in multiple other observational studies.16–18 This is supported by work performed by Maragkos and colleagues that identified a maximum aneurysm dome diameter ⩾15 mm as being independently associated with a higher rate of incomplete occlusion. 16
Aneurysm neck diameter and aneurysm-associated branch vessels were not independently associated with aneurysm retreatment in the current study. Results are mixed in the published literature regarding the role neck diameter plays in affecting aneurysm non-occlusion, with multiple groups reporting that neck diameter is not associated with residual aneurysm filling.19–21 Interestingly, Li and colleagues reported that a large aneurysm neck diameter was independently associated with aneurysm non-occlusion, 22 suggesting a need for further investigation. Multiple studies have demonstrated that incorporation of branch vessels into the aneurysm dome or neck is associated with non-occlusion.17,20,21,23 Although we did not observe an association between the incorporation of branch vessels into treated aneurysm angioarchitecture and need for future retreatment, this morphologic variable trended towards statistical significance on univariate analysis (p = 0.062), again raising the possibility that the current study was not sufficiently powered to detect this association.
There are several limitations that should be considered when interpreting the current findings. The retrospective nature of this study represents a major limitation. Patients included within the study cohort were recruited from tertiary care centers with significant clinical experience caring for individuals with complex cerebrovascular pathology, potentially introducing selection bias into our results and limiting study generalizability. The decision to treat, the techniques and equipment used for PED placement, and the antiplatelet regimen used were all operator dependent and not standardized across sites, potentially affecting outcomes. Despite this, we believe that the multicenter nature of the current study and variability in both interventional technique and patient management across sites provides more realistic insights into PED performance in diverse clinical practice settings. Over 98% of treated aneurysms evaluated in this study were in the anterior circulation, reflecting the fact that the PED is currently approved by the US Food and Drug Administration for treatment of intracranial aneurysms involving the petrous to superior hypophyseal ICA segments. This significantly limits the conclusions that can be drawn regarding determinants of retreatment for aneurysms involving the posterior and distal anterior circulation. The extent of aneurysm opacification was not well-evaluated in the current study, limiting the evaluation of effect that the volume of residual aneurysm filling has on retreatment. As in other published reports,24,25 aneurysms were classified as either completely or incompletely occluded, with aneurysm neck opacification receiving the same classification as aneurysm dome opacification. Lastly, clinical and angiographic outcome was self-reported and not assessed in a blinded fashion.
Conclusions
Prolonged use of DAPT for more than 12 months is a strong determinant of aneurysm retreatment, with large aneurysm dome diameter ( 10 mm) trending toward statistical significance in the current study. Considering these findings, close monitoring of the length of DAPT is important to ensure that its use is not prolonged, with the goal of discontinuing DAPT as soon as is reasonably possible to promote aneurysm occlusion. In cases requiring longer term DAPT, additional PED placement at the time of first procedure could be considered. Finally, larger aneurysms may be better served by placement of either multiple PEDs upfront or adjunct coiling.
Footnotes
Authors Note: Naif M Alotaibi is also affiliated with Department of Neurosurgery, National Neuroscience Institute, King Fahad Medical City, Riyadh, Saudi Arabia.
Conflict of interest: Justin R Mascitelli received compensation for lectures from Penumbra and PMI. Aman B Patel received compensation for consulting, device proctoring, and lecturing from Medtronic, Microvention, and Penumbra. Joshua Seinfeld received compensation for consulting from Medtronic.
Funding: The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the National Institutes of Health, National Institute of Neurological Disorders and Stroke (R25 NS065743).
ORCID iDs: Justin E Vranic https://orcid.org/0000-0002-6000-6709
Robert W Regenhardt https://orcid.org/0000-0003-2958-3484
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