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. 2024 Jul 21;38(2):133–141. doi: 10.1177/19714009241260805

Pipeline versus non-pipeline flow diverter treatment for M1 aneurysms: A systematic review and meta-analysis

Yigit Can Senol 1,✉, Atakan Orscelik 2, Cem Bilgin 2, Hassan Kobeissi 2, Sherief Ghozy 2, Santhosh Arul 2, David F Kallmes 2, Ramanathan Kadirvel 1
PMCID: PMC11571521  PMID: 39033417

Abstract

Background

The flow diversion treatment of aneurysms located distal to the Circle of Willis has recently increased in frequency. We conducted a systematic review and meta-analysis of the clinical and radiological outcomes of flow diverter (FD) embolization in treating M1 aneurysms.

Methods

PubMed, Web of Science, Ovid Medline, Ovid Embase, and Scopus were searched up to May 2024 using the Nested Knowledge platform. We included studies assessing the long-term clinical and radiological outcomes for M1 aneurysms. Results of FDs classified as Pipeline Embolization Devices (PED) versus other types of FDs. Angiographic occlusion rates, ischemic and hemorrhagic complications, and favorable clinic outcomes were included. All data were analyzed using R software version 4.2.2.

Results

Thirteen studies with 112 total patients (58 patients for PED and 54 patients for other FD devices) were included in our meta-analysis. The overall adequate (complete + near-complete) occlusion rates were 85.1%. The complete occlusion rate was higher with PED than with other FD devices (72.9% PED and 41.6% for non-PED FDs, respectively, p-value <.01). The ischemic complications were 9.9% and 9.0% for the PED and non-PED groups, respectively (p-value = .89). The overall modified Rankin Scale 0–2 was 100% for the non-PED and 97.1% for the PED group (p-value = .51). In-stent stenosis rate was 7.5% for PED devices compared to 2.6% in the non-PED group (p-value = .35).

Conclusions

This relatively small meta-analysis showed high rates of adequate and complete occlusion in FD treatment of M1 segment aneurysms, with favorable safety profiles. PEDs were associated with higher rates of complete aneurysm occlusion compared to other types of FDs.

Keywords: Pipeline, flow diverter, M1, aneurysm

Introduction

The off-label application of flow diverters (FDs) for treating intracranial complex aneurysms has recently increased in prevalence.1,2 However, FD therapy’s reliability and success rate for aneurysms located distal to the Circle of Willis, such as the M1 segment of the middle cerebral artery (MCA), remains uncertain.3–5 Studies have shown that FD treatment in small-diameter vessels is both effective and relatively safe, but the unique characteristics of M1 segment aneurysms may make them more challenging to treat with FDs.6,7

One relatively uncommon subgroup of distal aneurysms is the M1 segment of the middle cerebral artery (MCA), proximal to the MCA bifurcation, accounting for up to 16% of MCA aneurysms and up to 6% of all intracranial aneurysms. 8 Compared to bifurcation aneurysms, M1 segment aneurysms require a deeper dissection, and their intimate relationship with small branches can make clipping more complex. On the other hand, the small diameter parent artery and multiple perforating arteries might diminish enthusiasm for FD treatment of these M1 segment aneurysms.

Despite these challenges, the use of FDs for treating M1 segment aneurysms is of interest due to their high recurrence rate after conventional treatment. Therefore, the current study aims to provide meta-analytic data on the safety and efficacy outcomes of M1 aneurysms treated with FDs. We also pay special attention to insights into comparing pipeline embolization devices (PED; Medtronic, Irvine, California, USA) vs. other FDs. This will help determine if FD treatment is viable for this subgroup of distal aneurysms and to provide meta-analytic data regarding the safety and efficacy outcomes of M1 aneurysms treated FD.

Methods

This systematic review was written by the guidelines provided within the Preferred Reporting Items for Systematic Reviews and Meta-analyses (PRISMA) 2020 statement. We used the Autolit platform (Nested Knowledge, St Paul, Minnesota, USA) for conducting the literature search, duplicate removal, screening, and full-text screening.

Search strategy and selection criteria

Search strategies were created using a combination of keywords and standardized index terms. Searches were run on May 15, 2024; a literature search was conducted on Web of Science, PubMed, Scopus, and Embase using a combination of the terms (“M1 aneurysm” OR “M1 aneurysms” OR “MCA” OR “middle cerebral artery” OR “distal M1” OR “distal middle cerebral artery” OR “MCA aneurysm” OR “MCA aneurysms”) AND (“flow diverter” OR “flow diversion” OR “Pipeline” OR “Fred” OR “Fred JR” OR “Tubridge” OR “Silk” OR “Silk Vista” OR “Silk Vista Baby” OR “Surpass” “Phenox” OR “P64” OR “P48”). Moreover, we did an extensive manual search through the articles’ references to retrieve any additional articles.

Screening and study selection

The inclusion criteria were English language, M1 aneurysm treatment with flow diverter devices, and data availability on M1 aneurysm treatment complications and outcomes. Only aneurysms that have an origin in the M1 segment are included. Aneurysms internal carotid artery (ICA) or MCA bifurcations treated by FDs extended to the M1 segment are excluded. Both noncomparative (articles solely focused on M1 aneurysm treatment with Pipeline flow diverters) and comparative studies (articles comparing Pipeline flow diverters with flow diverters) were included in the meta-analysis.

Literature reviews, systematic reviews, meta-analyses, case reports, and case series consisting of <3 patients, abstracts, conference papers, and in vitro studies were excluded. Articles focused on Flow diverted treatment on M1 segment aneurysms and articles do not providing separate outcomes for M1 aneurysm treatment with FDs were also excluded. Additionally, studies that used different types of FDs in the same aneurysm were excluded. The authors completed the initial title and abstract screening independently. Duplicates and overlapping data (studies published on the same registry) were omitted. Next, two investigators independently performed the full-text screening (YCS, AO). In case of conflict, the senior author (DFK with more than 20 years of experience) resolved the disagreement. The literature search, initial and full-text screening, and data extraction were performed with the AutoLit platform (Nested Knowledge, St Paul, Minnesota, USA).

Data extraction

We extracted the aim and the summary of the included studies, the FD device used, the study design, and different treatment outcomes. We had all original studies fulfilling our pre-determined Population/Intervention/Control group/Outcome (PICO). The population was patients with M1 aneurysms; the Intervention was flow diverter treatment; the Control group was Pipeline Flow diverters; Outcomes of interest were complete occlusion, near plus complete occlusion, in-stent stenosis, ischemic complications, hemorrhagic complications, and favorable outcomes.

Quality assessment

For quality assessment for our observational non-randomized included studies, we used the Risk Of Bias In Non-Randomized Studies—of Interventions (ROBINS-I) tool to assess the risk of bias. Based on seven domains, studies with a “Low,” “Moderate,” “Serious,” or “Critical” risk of bias were examined and appraised (confounding bias, selection bias, measurement classification of interventions bias, deviation from intended intervention bias, missing data bias, measurement of outcomes bias, and selection of the reported result bias. Quality assessments were completed separately by two authors (YS, SA). Discussions between the two authors were successful in resolving any disagreements of opinion.

Outcome variables

Raymond–Roy occlusion classification (RROC) 1 and O'Kelly-Marotta (OKM) D results were defined as aneurysm total occlusion. RROC 1 + 2 and OKM C + D are defined as adequate occlusion. Good clinical outcome was defined as a modified Rankin Scale (mRS) score of 0-2 for at least 90 days or a Glasgow Outcome Score (GOS) of 4 at discharge. Any deterioration in mRS or GOS scores was not considered a good clinical outcome, even if the mRS score was 1–2 or the GOS score was 4. Hemorrhagic complications were described as new or worsening intracranial and extracranial hemorrhage, including groin hematoma, genitourinary, or gastrointestinal bleeding. Any imaging-proven ischemic events were defined as thromboembolic complications. Silent ischemic infarcts on radiological images were excluded from ischemic complications. In these studies, clinically significant or silent ischemic complications were included. We included all patients identified with moderate in-stent stenosis (>50%) and those with mild in-stent stenosis who were symptomatic during their initial angiographic follow-up. If in-stent stenosis increased at their latest radiological follow-ups, even if asymptomatic, these flow diverters were considered as in stent-stenosis.

Statistical analysis

Using R software version 4.2.2, we calculated pooled prevalence rates and their corresponding 95% confidence intervals (CI). A random model was adopted to pool all data due to methodological heterogeneity among the included studies. Data pooling was done using log transformation, except for outcomes with multiple zero events, Arcsine transformation was used instead. Heterogeneity was assessed using Q statistics and the I2 test, where I2 > 50% or p-value <.05 were considered significant. Moreover, we did a subgroup analysis to compare the outcomes of using PED and non-PED devices. Among the compared subgroups, the number of studies was less than ten, so, publication bias (Egger’s regression test) and the impact of sample size (meta-regression) were not tested.

Results

Search results

In total, 1021 articles in the literature were screened according to their titles and abstracts. As a result of this initial screen, 994 entries were excluded. The remaining 27 articles were read in full text, and 14 more studies were excluded as they were unrelated to our inclusion criteria. A systematic review was prepared with the remaining thirteen studies. Four studies have both results for multiple flow diverters (Supplemental Figure 1). Six studies involved the Pipeline Embolization Device (PED, Medtronic, Irvine, California, USA) with 58 patients with 58 aneurysms, and six studies with 54 patients with 54 aneurysms constituted the non-PED group. The FDs used in the Non-Ped group were P64(Phenox GmbH, Germany), P64(HPC) (Phenox GmbH, Germany), Tubridge (MicroPort Medical Company, Shanghai, China), Silk Vista Baby (Balt Extrusion, Montmorency, France), and Fred Jr(MicroVention, Tustin, California) Three studies were evaluated as having a moderate risk of bias, while the remaining ten were assessed as having a low risk of bias (Supplemental Figure 2).

Study characteristics and descriptive overview

A total of 115 patients were included in the studies at the starting point, and 112 patients were eligible in our inclusion criteria for analysis. Three patients were excluded due to the overlapping deployment of two different flow diverters in the same session. Three were multicenter cohort studies; the remaining ten were single-center studies. Studies summarized in Table 1.

Table 1.

Study Description.

Authors Years Centers Study Design Patient Number Aneurysm Number Female Gender Anti-platelet Regimen Follow-up Time(Average) Rupture Status Flow Diverter Country
Bhogal et. al. 2009-2016 Single Retrospective 15 15 11/15(%73) Aspirin+ clopidogrel(if there is poor respond for clopidogrel switched to ticagrelor) 18.7 months Unruptured P64 (Phenox, Germany), PED (Medtronic, USA) Germany
Lauzier et. al. 2011-2020 Multi Retrospective 17 17 - Aspirin+ clopidogrel(if there is poor respond for clopidogrel switched to ticagrelor) 30 months (range 1–74 months) 1/17(5.8%) PED (Medtronic, USA) USA
Li et. al. 2017-2020 Single Retrospective 12 12 6/12(%50) Aspirin + Clopidogrel 10 ± 7 months 1/12(8.3%) Tubridge (MicroPort, China), PED (Medtronic, USA) China
Martinez Galdimez et. al. - Multi Retrospective 11 11 - Aspirin+ clopidogrel(if there is poor respond for clopidogrel switched to ticagrelor) 6 months 1/11(9%) PED (Medtronic, USA) Spain, USA
Schob et. al. 2018 Single Prospective 3 3 - Aspirin+Ticagrelor 1.3 Months (First DSA Follow-Up – Only one aneurysm had incomplete occlusion) Unruptured Silk Vista Baby (Balt, France) Germany
Yu et. al. 2015-2019 Single Retrospective 6 6 3/6(%50) Aspirin+ clopidogrel(if there is poor respond for clopidogrel switched to ticagrelor) 10.9 ± 11.4 months 1/6(16.6%) PED (Medtronic, USA) China
Mohlenbruch et. al. 2015-2016 Multi Retrospective 5 5 4/5(%90) 2 center Dual(aspirin+ clopidogrel)/ 2 centers mono with prasugrel 6 or 12 months follow-up for all patients Unruptured Fred Jr (MicroVention, USA) Turkey, Germany, Austria
Hellstern et. al. 2020-2021 Single Retrospective 11 11 - Prasugrel 56 days Unruptured P64 (Phenox, Germany) Germany
Liang et. al. 2018-2019 Single Prospective 3 3 1/3(%33) Aspirin+ clopidogrel(if there is poor respond for clopidogrel switched to ticagrelor) 7.5 ± 4.0 months Only 1 aneurysm ruptured 1 month before Tubridge (MicroPort, China) China
Monteith et. al. 2011-2013 Single Retrospective 6 6 1/6(%16) Aspirin + Clopidogrel 6.3 months Unruptured PED (Medtronic, USA) USA
Zanaty et. al. 2010-2013 Single Retrospective 5 5 - Aspirin+ clopidogrel(if there is poor respond for clopidogrel switched to prasugrel) 7.55 months Unruptured PED (Medtronic, USA) USA
Gai et. al. 2018-2023 Single Retrospective 10 10 5(50%) Aspirin+ clopidogrel(if there is poor respond for clopidogrel switched to ticagrelor) 22.7 months Unruptured PED (Medtronic, USA), Tubridge (MicroPort, China), Surpass Evolve(Stryker, USA) China
Yan et. al. 2018-2022 Single Retrospective 11 11 6/11(54%) Aspirin and clopidogrel OR ticagrelor 22.36 ± 13.97 months Unruptured PED (Medtronic, USA), Tubridge (MicroPort, China) China
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Angiographic outcomes

The analysis included a total of 108 patients and the studies showed rate of adequate occlusion at 85.1% (95% CI = 74.3–95.9), with significant heterogeneity (I 2 = 63%; p-value <.05). Patients treated with PED devices achieved significantly higher rates of adequate occlusion compared to those treated with non-PED devices (98.9%, 95% CI = 93.2–100 versus 67.8%, 95% CI = 50.4–85.2, respectively, p-value <.01) (Figure 1).

Figure 1.

Figure 1.

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Forest plot of adequate occlusion rates.

The overall rate of complete occlusion was 59.9% (95% CI = 46.1–73.1), with significant heterogeneity (I2 = 67%; p-value <.01). The PED group had a significantly higher rate of complete occlusion compared to the non-PED group (72.9%; 95% CI = 55.2–90.5 versus 41.6%; 95% CI = 29–54.3, respectively, p-value <.01) Furthermore, significant heterogeneity was found in the PED group (I2 = 60%, p-value = .01), despite the non-PED group (I2 = 0%, p-value = .64). (Figure 2).

Figure 2.

Figure 2.

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Forest plot of complete occlusion rates.

Ischemic complications

The study analyzed a total of 112 patients and found an ischemic complication rate of 9.4% (95% CI = 3.5–15.3) with no significant heterogeneity (I2 = 0%; p-value = .74). No significant difference was found in the ischemic complications between the PED and non-PED groups (p-value = .89), and there was no significant heterogeneity in either group (PED: I2 = 0%, p-value = .77; non-PED: I2 = 6%, p-value = .39) (Figure 3).

Figure 3.

Figure 3.

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Forest plot of ischemic complication rates.

Clinical outcomes

Good clinical outcome was achieved in 109 of 112 patients with 98.8% (95% CI = 94.7–100), and no heterogeneity was observed (I2 = 0%; p-value = .973). 2 of 3 patients had a PED occlusion in postoperative 1 month and these patients had basal ganglia infarct reported in Lauzier et. al. 9 The other patient had stopped anti-platelet drugs before the final date and had a stroke reported in Zanaty et. al. 10 The overall favorable clinical outcome was comparable between patients treated with PED (97.1%; 95% CI = 90.6–100) and those treated with non-PED devices (100%; 95% CI = 95.6–100) (p-value = .50) (Figure 4), no heterogeneity was found in either group (PED: I2 = 0%, p-value = .95; non-PED: I2 = 0%, p-value >.99). Among the non-PED devices, all devices achieved 100% good clinical outcomes.

Figure 4.

Figure 4.

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Forest plot of mRS 0–2.

In-stent stenosis

The analysis included a total of 112 patients, and the pooled rate of in-stent stenosis was 4.5% (95% CI = 0–9.38), but there was no significant heterogeneity (I2 = 5%; p-value = .039) among the studies included in the analysis. In terms of in-stent stenosis rates, there was no significant difference (p-value = .35) between those treated with PED (7.5%, 95% CI = 0.00–15.41) and non-PED devices (2.6%, 95% CI = 0.00–8.86) (Figure 5).

Figure 5.

Figure 5.

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Forest plot of in-stent stenosis rates.

Hemorrhagic complications

A total of 112 patients were analyzed, and hemorrhagic complication rate was 0.46% (95% CI = 0.00–4.3) with no heterogeneity (I2 = 0%; p-value >.95). There was no significant difference between the PED and non-PED groups in terms of hemorrhagic complications (p-value >.95), and no heterogeneity was observed in either group (PED: I2 = 0%, p-value = .78; non-PED: I2 = 0%, p-value >.95) (Online Supplemental Figure 3). In the case of non-PED devices, no hemorrhagic complications were reported in the included studies. Only one case reported in the PED devices group which is reported as distal perforation with the microwire during the exchange maneuver. 11

Discussion

In this relatively small meta-analysis of the use of FD in treating M1 segment aneurysms, we found that rates of adequate and complete occlusion were relatively high and that adverse events were low. We provide the first report of collective evidence for FD treatment for M1 aneurysms. Our results show a pooled complete occlusion for all FDs in rate of 59.9%. The favorable outcome was achieved in 98.8% of all included patients, with an ischemic events rate of 9.4%. Instances of ischemic stroke were not noticeably lower, even in the setting of multiple perforating arteries, and rates of in-stent stenosis were low. These findings may guide therapy in patients harboring M1 segment aneurysms, given the promising efficacy and safety outcomes presented.

Recent randomized clinical trial studies comparing surgical clipping over endovascular coiling in MCA aneurysms have shown that surgical management improved angiographic and clinical outcomes than endovascular coiling.12,13 Similarly, a recent meta-analysis focused on the treatment of MCA aneurysms found that surgical clipping was associated with higher rates of complete occlusion (76.7% vs. 56.6%, respectively) and better clinical outcomes (82.7% vs. 73.2%) in surgical clipping compared to endovascular coiling, respectively.14,15 However, when it comes to M1 aneurysms, surgical clipping can be more challenging as it requires more brain retraction and careful inspection for hidden perforating branches arising from the M1 segment. 16 Surgical clipping of M1 aneurysms presents technical challenges, which has led to the exploration of endovascular techniques as an alternative treatment option. However, there is currently no agreement in the literature on which treatment modality is superior for M1 aneurysms. It has been observed that endovascular coiling is not as effective as surgical clipping for MCA aneurysms, which has prompted the use of stent-coiling and flow diverters in MCA aneurysms. 17 The use of FDs in MCA aneurysms has increased in recent years, as they have similar complication rates with primary coiling, 18 fewer complications, and significantly better results in wide-neck aneurysms compared to stent-assisted coiling. 19 Currently, there is limited research focusing specifically on the use of flow diverter (FD) treatments for M1 aneurysms, and existing knowledge is mostly derived from treating MCA aneurysms as a whole. In a recent meta-analysis published in 2017 that included 244 MCA aneurysms, the rate of adequate occlusion was reported as 78% with a permanent complication rate of 10%. Our study, which focused on FD treatment of M1 aneurysms, showed even better angiographic outcomes, with an 85.1% rate of adequate occlusion, and a similar rate of complications at 9.4%.

The use of low-profile or small flow diverters for the treatment of distal cerebral aneurysms beyond the circle of Willis has recently increased in popularity. Previous meta-analyses have studied the use of FDs in distal aneurysms, including anterior cerebral artery and MCA with fewer complications and high success rates.20,21 In contrast, complex bifurcations may benefit from surgical procedures over flow diverters. 22 With the introduction of low-profile flow diverters into daily use, revolutionary developments have occurred in treating aneurysms located beyond Willis’s circle. Previous studies reported good clinical and angiographic outcomes in the use of low-profile flow diverters, especially in wide neck aneurysms with small parent artery diameters.23,24 Additionally, several studies demonstrated that PEDs are also have good clinical and angiographic outcomes on treatment of small cerebral vessels.25,26 Our meta-analysis reported that PEDs have better angiographic outcomes and comparable clinical outcomes over other FDs. The primary reason behind the outcomes may be related to popularity of the PED which was the first device to be introduced in USA market, leading the way for wider usage of flow diverters. As more research is conducted and more experience is gained in the use of other devices, their effectiveness and safety in treating distal cerebral aneurysms are becoming better understood, contributing to the growth in their use. The FDs’ long-term safety and efficacy for treating M1 aneurysms are excellent. In addition, the technical features of flow diverters also differ. Pipeline, FRED, Surpass, p48, and p64 flow diverters offer distinct technical features for endovascular treatment of intracranial aneurysms. Pipeline flow diverters, made of a low-porosity braided cobalt-chromium and platinum alloy mesh, conform well to vessel anatomy and provide optimal blood flow diversion. 27 The FRED system features a self-expanding, dual-layer design with a high-porosity outer stent and a low-porosity inner mesh for improved flow diversion and precise placement. 28 Surpass flow diverters, made from a cobalt-chromium alloy with a braided mesh design, offer high radial force for better wall apposition and aneurysm occlusion. 29 Both p48 and p64 flow diverters use a nitinol-based mesh; however, p48 is coated with a hydrophilic polymer, which enhances navigability, while p64 has a unique design that combines a flow diverter with an integrated, detachable web, offering advantages in treating bifurcation aneurysms. 30 Each of these devices presents a different approach to flow diversion, catering to various clinical scenarios and aneurysm characteristics. However, further prospective studies with larger sample sizes are needed to fully determine FDs’ feasibility and safety.

Our meta-analysis has several substantial limitations. First, the total number of patients was small which reduced the statistical power. Second, all included studies were non-randomized, noncomparative case series and selection bias is inevitable. Third, there likely was substantial heterogeneity in terms of the clinical status of patients and use of devices. Fourth, due to the limited availability of literature on the use of flow diverters (FDs) for the treatment of M1 aneurysms specifically, the non-PED group was compared to the PED group as a single entity. As a result, the outcomes of the non-PED group showed a high degree of heterogeneity. In addition, the baseline characteristics varied across the included studies.

Conclusion

This relatively small meta-analysis showed high rates of adequate and complete occlusion in FD treatment of M1 segment aneurysms, with favorable safety profiles. Ultimately, PEDs are slightly better in treatment of M1 aneurysms with low complications rates with high complete occlusion rates than other FDs. Future prospective studies are needed to validate these findings and directly compare the safety and feasibility of different FDs in treatment of M1 aneurysms.

Supplemental Material

Supplemental Material - Pipeline versus non-pipeline flow diverter treatment for M1 aneurysms: A systematic review and meta-analysis
sj-pdf-1-neu-10.1177_19714009241260805.pdf (1.9MB, pdf)

Supplemental Material for Pipeline versus non-pipeline flow diverter treatment for M1 aneurysms: A systematic review and meta-analysis by Yigit Can Senol, Atakan Orscelik, Cem Bilgin, Hassan Kobeissi, Sherief Ghozy, Santhosh Arul, David F Kallmes and Ramanathan Kadirvel in The Neuroradiology Journal.

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding: The author(s) received no financial support for the research, authorship, and/or publication of this article.

Supplemental Material: Supplemental material for this article is available online.

ORCID iDs

Yigit Can Senol https://orcid.org/0000-0002-6669-6616

Atakan Orscelik https://orcid.org/0000-0001-6481-3076

Cem Bilgin https://orcid.org/0000-0003-1832-1278

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Supplementary Materials

Supplemental Material - Pipeline versus non-pipeline flow diverter treatment for M1 aneurysms: A systematic review and meta-analysis
sj-pdf-1-neu-10.1177_19714009241260805.pdf (1.9MB, pdf)

Supplemental Material for Pipeline versus non-pipeline flow diverter treatment for M1 aneurysms: A systematic review and meta-analysis by Yigit Can Senol, Atakan Orscelik, Cem Bilgin, Hassan Kobeissi, Sherief Ghozy, Santhosh Arul, David F Kallmes and Ramanathan Kadirvel in The Neuroradiology Journal.

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