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Effect of Straightening the Parent Vessels in Stent-Assisted Coil Embolization for Anterior Communicating Artery Aneurysms
Original Article
Effect of Straightening the Parent Vessels in Stent-Assisted Coil Embolization for Anterior Communicating Artery Aneurysms Yusuke Funakoshi1, Hirotoshi Imamura1, Shoichi Tani1, Hidemitsu Adachi1, Ryu Fukumitsu1, Tadashi Sunohara1, Keita Suzuki1, Yoshihiro Omura1, Yuichi Matsui1, Natsuhi Sasaki1, Toshiaki Bando2, Tatsumaru Fukuda1, Ryo Akiyama1, Kazufumi Horiuchi1, Shinji Kajiura1, Masashi Shigeyasu1, Nobuyuki Sakai1
BACKGROUND: Stent-assisted coil embolization (SAC) for treating anterior communicating artery (AcomA) aneurysms is safe and effective. Straightening of parent vessels by stent placement can lead to progressive thrombosis. We describe our experience with SAC for AcomA aneurysms and demonstrate the effect of straightening the parent vessels.
-
METHODS: A total of 26 patients with AcomA aneurysms were treated using SAC in our institute between July 2010 and December 2017. Follow-up digital subtraction angiography was performed 6 months after treatment, magnetic resonance angiography was performed every year, and outcomes were analyzed.
was significant at the 6-month follow-up. The median followup term was 18 months. No patients required retreatment. CONCLUSIONS: Good SAC outcomes were achieved for AcomA aneurysms, and hemodynamic changes related to straightening of the parent vessels is a consideration in SAC.
-
-
RESULTS: From all aneurysms (n [ 24), 12 (50.0%) were neck remnant, and 12 (50.0%) were dome-filling types immediately after the procedure. At the 6-month digital subtraction angiography follow-up (n [ 22), 13 (59.1%) aneurysms were complete obliteration, 8 (36.4%) were neck remnant, and 1 (4.5%) was dome filling. The median parent vessel angle was measured preoperatively at 98.1 , increased to 124.8 immediately after stent deployment, and further increased to 149.6 at the 6-month follow-up. Progressive thrombosis was observed in 13 of 22 (59.1%) aneurysms. The parent vessel angle change immediately after stent deployment in the progressive thrombosis group tended to be larger than that observed in the no thrombosis group; this change
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Key words Aneurysmal stenting - Anterior communicating artery - Progressive thrombosis - Stent-assisted coil embolization - Straightening of parent vessels -
Abbreviations and Acronyms AcomA: Anterior communicating artery CFD: Computational fluid dynamics CO: Complete obliteration DF: Dome filling DSA: Digital subtraction angiography MRA: Magnetic resonance angiography mRS: Modified Rankin Scale
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INTRODUCTION
S
tent-assisted coil embolization (SAC) is a preferred technique in the treatment of wide-neck intracranial aneurysms. Stent-assisted techniques make it possible to preserve the parent vessels and perform sufficient coil embolization of aneurysms, which are technically difficult to treat. Furthermore, straightening of the parent vessels and the stent strut itself have been shown to alter hemodynamics in both bifurcation-type1 and sidewall-type aneurysms,2 based on computational fluid dynamics (CFD) studies. Neck-bridging stents have been widely indicated for wide-neck intracranial aneurysms, and SAC has provided higher rates of complete occlusion and low rates of recanalization in longterm follow-up studies compared with coiling alone.3-6 Anterior communicating artery (AcomA) aneurysms have anatomic features that differ from internal carotid artery aneurysms. In the past, AcomA aneurysms were difficult to treat with coil embolization because endovascular treatment was limited by the typically small diameter and acute angles of the parent
NR: Neck remnant SAC: Stent-assisted coil embolization VER: Volume embolization ratio From the 1Department of Neurosurgery, Kobe City Medical Center General Hospital, Kobe City; and 2Department of Neurosurgery and Stroke Center, Shinko Hospital, Kobe City, Japan To whom correspondence should be addressed: Yusuke Funakoshi, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.02.066 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
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ORIGINAL ARTICLE YUSUKE FUNAKOSHI ET AL.
STENT-ASSISTED COIL EMBOLIZATION FOR ACOMA ANEURYSMS
vessels.7-9 However, such aneurysms have been rendered treatable by the development of endovascular techniques and devices such as newer microguidewires or catheters and by balloon-assisted or stent-assisted coiling.3,5,10 Recently, stent-assisted coil embolization for AcomA aneurysms has been widely indicated, and the effect of straightening the parent vessels and the resulting hemodynamic changes mediated by stent placement have been a research focus.11 AcomA complexes can be mobilized by stent placement because the complexes are not fixed to osseous structures and they have characteristics such as small diameters and thin vessel walls. Data are insufficient to determine the ramifications of the effect of straightening a parent vessel in SAC for AcomA aneurysms. Although a CFD study may be necessary for full evaluation, CFD study has been used in only a few clinical cases. In this report, we describe our experience using SAC for AcomA aneurysms and describe the effect of straightening the parent vessels, based on parent vessel angle changes.
Table 1. Patient Characteristics (N ¼ 24) Age (years)
63 (55e70)
Sex Female
9 (37.5%)
Male
15 (62.5%)
Background Smoke
13 (54.2%)
HT
13 (54.2%)
DL
7 (29.2%)
DM
2 (8.4%)
Aneurysm dome (mm)
7.3 (6.8e8.0)
Aneurysm neck (mm)
4.9 (3.8e5.6)
Ruptured aneurysm
1 (4.2%)
Median (interquartile range). HT, hypertension; DL, dyslipidemia; DM, diabetes mellitus.
MATERIALS AND METHODS Characteristics of Patients and Aneurysms A total of 24 consecutive patients (9 women and 15 men) with AcomA aneurysms were treated in our institute using SAC between July 2010 and December 2017. We excluded all patients undergoing repeated aneurysmal therapy. Indications for SAC included aneurysm neck size >4 mm, unfavorable dome-to-neck ratio <2, coil instability, or a decision by the senior neurosurgeon that simple coiling, balloon-assisted techniques, or the double-catheter technique were inadequate treatment approaches. Patients’ characteristics are summarized in Table 1. The median patient age was 63 years; 13 patients (54.2%) were smokers, and 13 (54.2%) had previously received diagnoses of hypertension. The median aneurysm dome diameter was 7.3 mm, and the median aneurysm neck diameter was 4.9 mm. The study contained 1 (4.2%) patient with a previously ruptured aneurysm.
Since 2015 we have most often used a hybrid braided closed-cell stent, LVIS Jr. (MicroVention-Terumo, Tustin, California, USA) as a successor to the Neuroform EZ stent. The Neuroform Atlas (Stryker Neurovascular, Fremont, California, USA) is now used to treat aneurysms in small parent vessels with acute angles. Coiling was performed immediately after stent deployment through the microcatheter, which either was placed inside the aneurysm before stent deployment and jailed between the stent and the vessel wall (jailing technique) or was advanced through the stent struts after stent deployment (trans-cell technique). The volume embolization ratio
Perioperative Antiplatelet Management Dual antiplatelet therapy with aspirin and clopidogrel is generally performed for SAC in our institute. Patients took 100 mg aspirin and 75 mg clopidogrel daily for at least 7 days before SAC. Antiplatelet activity was assessed using aspirin and P2Y12 assays (VerifyNow; Accumetrics, San Diego, California, USA) the day before the procedure. When aspirin reaction unit measurements were >550, aspirin was increased to 200 mg. When P2Y12 reaction unit measurements were >220, a loading dose of 20 mg prasugrel was given, and prasugrel was decreased to 3.75 mg once per day, the following day. In patients showing no resistance to antiplatelet therapy, clopidogrel was decreased gradually, beginning 6 months after the procedure, and was discontinued after 1 year. Aspirin was continued as a lifelong treatment. Endovascular Procedures All patients received heparin after an arterial puncture, to maintain increased activated clotting time at approximately 300 seconds during the procedure. Initially, open-cell Neuroform EZ (Stryker Neurovascular, Kalamazoo, Michigan, USA) and closed-cell Enterprise (Cordis Neurovascular Inc., Miami, Florida, USA) stents were used.
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Figure 1. Measurement of the angle between 2 lines, which was approximated as a straight line passing through the center of the parent vessels, from 3-dimensional data derived from digital subtraction angiography and y use of Mimics and 3-matic software (Materialize Japan, Yokohama, Japan).
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ORIGINAL ARTICLE YUSUKE FUNAKOSHI ET AL.
STENT-ASSISTED COIL EMBOLIZATION FOR ACOMA ANEURYSMS
(VER) was measured after the procedure, and the parent vessel angles were measured using 3-dimensional data obtained from digital subtraction angiography (DSA) with Mimics and 3-matic software (Materialize Japan, Yokohama, Japan) (Figure 1) before the procedure, immediately afterward, and at the 6-month follow-up (Figure 2).
across the necks of all 24 aneurysms, and the median VER of the aneurysms was 27.4%. Among all aneurysms (n ¼ 24), 12 (50.0%) were NR, and 12 (50.0%) were DF immediately after the procedure. At the 6-month DSA follow-up (n ¼ 22), 13 (59.1%) were CO, 8 (36.4%) were NR, and 1 (4.5%) was DF. No patients required retreatment for recanalization during follow-up. The preoperative median parent vessel angle was 98.1 (n ¼ 24), which increased to 124.8 immediately after stent deployment (n ¼ 24) and further increased to 149.6 at the 6-month follow-up (n ¼ 22). Angle changes immediately after stent deployment with each type of stent are shown in Table 3. The median angle change was 33.6 for the Enterprise stent (n ¼ 7), 23.7 for the Neuroform EZ stent (n ¼ 7), 34.1 for the LVIS Jr. stent (n ¼ 6), and 7.7 for the Neuroform Atlas stent (n ¼ 4). Angle changes after stent deployment for each type of stent were significantly different (P ¼ 0.0417). Factors related to progressive thrombosis are shown in Table 4. Progressive thrombosis was observed in 13 of 22 (59.1%) aneurysms. There was no significant difference in aneurysm dome diameter, aneurysm neck diameter, and VER. The median parent vessel angle change immediately after the procedure in the progressive thrombosis group was 33.6 , which tended to be larger than the 17.1 observed in the no thrombosis group (P ¼ 0.0662). Median angle change at the 6month follow-up in the progressive thrombosis group was significantly larger than that in the no thrombosis group (P ¼ 0.0177). Logistic regression analysis was performed to assess aneurysm neck diameter and parent vessel angle change immediately after the procedure. Results were not significant but tended toward significance in univariate analysis, and both factors may be useful intraoperative factors related to progressive thrombosis (Table 5). Although there was no significant difference for aneurysm neck (P ¼ 0.4062), there was a tendency toward significance for parent vessel angle change (P ¼ 0.0594).
Follow-Up Angiographic results were classified as complete obliteration (CO), neck remnant (NR), and dome filling (DF). Any further filling of the aneurysm sac over time was referred to as recanalization in follow-up DSA or magnetic resonance angiography (MRA). “Progressive thrombosis” meant that aneurysms that were NR or DF immediately after the procedure changed to CO in follow-up DSA. Follow-up DSA was performed 6 months after treatment, and follow-up MRA, using 1.5-T magnet strength, was performed every year. In patients with recanalization, we scheduled retreatment or earlier follow-up DSA. Statistical Analysis Statistical analysis was conducted using JMP software (version 10, SAS Institute, Cary, North Carolina, USA). VER and parent vessel angle changes were analyzed using the Fisher exact test and the Mann-Whitney U test. Results of the logistic regression model were presented as odds ratio, 95% confidence interval, and P value. P < 0.05 was considered statistically significant. RESULTS Embolization Results and Parent Vessel Angle Changes Study outcomes are summarized in Table 2. The median follow-up term was 18 months. Stent wall apposition was verified using conebeam computed tomography. Stents were successfully deployed
Figure 2. 3-dimensional digital subtraction angiographic images showing the parent vessel angles (A, before treatment; B, immediately after treatment; C, 6-month follow-up). Straightening of the parent vessels is
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visible. White arrowhead, coiled aneurysm; white arrows, distal and proximal stent markers.
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STENT-ASSISTED COIL EMBOLIZATION FOR ACOMA ANEURYSMS
Table 2. Outcomes of DSA After SAC and Factors Related to Recanalization VER (%)
Table 4. Factors Related to Progressive Thrombosis
Factor
Progressive Thrombosis (n [ 13)
No Thrombosis (n [ 9)
P Value
7.0 (6.4e7.5)
7.8 (5.9e8.3)
0.2426
27.4 (21.0e34.3)
Initial DSA outcome (n ¼ 24) CO
0 (0.0%)
Aneurysm dome (mm)
NR
12 (50.0%)
Aneurysm neck (mm)
4.1 (3.7e5.1)
5.1 (4.4e7.1)
0.1089
12 (50.0%)
VER (%)
33.7 (19.2e36.7)
24.1 (22.3e29.5)
0.171
Postoperative angle change ( )
33.6 (23.6e57.1)
17.1 (5.9e32.5)
0.0662
6-month angle change ( )
57.0 (42.2e86.3)
33.5 (26.9e51.8)
0.0177
DF 6-month DSA outcome (n ¼ 22) CO
13 (59.1%)
NR
8 (36.4%)
DF
1 (4.5%) Median (interquartile range). VER, volume embolization ratio.
Parent vessel angle ( ) Preoperative
98.1 (84.0e107.6)
Immediately after
124.8 (107.2e135.6)
6-month follow-up
149.6 (140.0e155.5)
Recanalization
0 (0.0%)
Follow-up (months)
18 (9e41)
Median (interquartile range). DSA, digital subtraction angiography; SAC, stent-assisted coil embolization; VER, volume embolization ratio; CO, complete obliteration; NR, neck remnant; DF, dome filling.
Complications Complications are shown in Table 6. As a procedure-related complication, asymptomatic thromboembolism was observed in 12 patients (50.0%). Although symptomatic thromboembolism was observed in 1 patient (4.2%), this symptom was transient. No aneurysmal ruptures were observed in our study. Complications unrelated to the procedure included hemorrhage from gastric ulcer and hemodynamic cerebral infarction in 1 patient (4.2%). Disuse syndrome caused worsening of the modified Rankin Scale (mRS) in 1 patient (4.2%). At the final follow-up, the mRS was worse in only 1 patient, who had disuse syndrome, and we saw no change in mRS in the remaining patients.
with a high rate of complete angiographic occlusion.10 In this study, the rates of immediate and long-term complete and nearcomplete angiographic occlusion were 88% and 85%. The retreatment rate was 7%, and overall procedure-related morbidity and mortality were 6% and 3%. Endovascular treatment for AcomA aneurysms has developed with a high degree of safety and efficacy. Kocur et al.12 reviewed 3 stent-assisted coil embolizations for AcomA aneurysms and showed that the complete and nearcomplete occlusion rate was 66% to 95% initially and 88% to 95% at follow-up. Johnson et al.5 observed progressive thrombosis at the 6-month follow-up in 17 of 27 (63%) patients with initially incomplete occlusion after SAC for AcomA aneurysms. Because arterial wall reconstruction by stent endothelialization and hemodynamic changes are considered to cause progressive thrombosis,3,6,13 we focused on the effect of straightening the parent vessels as a clinically assessable index. In our study, although the complete angiographic obliteration rate was 0.0% initially, the rate improved to 59.1% at the 6-month follow-up. The median preoperative parent vessel angle was 98.1 , which increased to 124. 8 immediately after stent deployment and further increased to 149.6 at the 6-month follow-up. Progressive thrombosis and parent vessel angle change, and secondary hemodynamic changes can be characteristics of treatment for AcomA aneurysms.
DISCUSSION SAC for AcomA Aneurysms A meta-analysis published in 2014 evaluating coil embolization of AcomA aneurysms showed that coil embolization is associated Table 3. Parent Vessel Straightening Effects for Each Type of Stent Angle Change ( )
P Value
Enterprise (n ¼ 7)
33.6 (26.7e34.2)
0.0417
Neuroform EZ (n ¼ 7)
23.7 (7.1e33.2)
LVIS Jr. (n ¼ 6)
34.1 (21.8e74.3)
Stent Type
Neuroform Atlas (n ¼ 4)
7.7 (2.5e17.7)
Median (interquartile range).
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Progressive Thrombosis Secondary to Straightening Effect of Parent Vessels Cho et al.14 reported that progressive thrombosis is often seen in aneurysms with small neck diameters or high coil packing density
Table 5. Logistic Regression Analysis of Aneurysm Neck Diameter and Parent Vessel Angle Change Immediately After Stent-Assisted Embolization Variable Aneurysm neck (1-mm increments)
Postoperative angle change (1 )
Odds Ratio
95% CI
P Value
0.79
0.37e1.34
0.4062
1.05
0.99e1.14
0.0594
CI, confidence interval.
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ORIGINAL ARTICLE YUSUKE FUNAKOSHI ET AL.
STENT-ASSISTED COIL EMBOLIZATION FOR ACOMA ANEURYSMS
Table 6. Complications and Modified Rankin Scale Score After Stent-Assisted Coil Embolization Complication
Number (%)
Procedure-related complication Asymptomatic thromboembolism
12 (50.0)
Symptomatic thromboembolism
1 (4.2)
Aneurysm rupture
0 (0.0)
resulting from the straightening of the parent vessels can be a factor contributing to treatment outcomes, although other factors certainly may be related to aneurysm occlusion. Because progressive thrombosis is expected in AcomA aneurysms treated by SAC, aggressive coil packing is unnecessary. In addition, parent vessel angle changes are significantly different for each type of stent. Although the effect of straightening the parent vessels is higher with closed-cell stents, we should consider that placing these stents is often difficult when the parent vessel angle is too sharp or the parent vessel diameter is too small.
Other complication Gastrointestinal hemorrhage
1 (4.2)
Disuse syndrome
1 (4.2)
Preoperative mRS 0
22 (91.7)
1e2
2 (8.3)
3e5
0 (0.0)
Last mRS 0
22 (91.7)
1e2
1 (4.2)
3e5
1 (4.2)
and in nonbranching aneurysms. SAC also has advantages regarding the progressive thrombosis rate and lower recurrence rate.11,15 A CFD study revealed that angular remodeling by the straightening effect displaces and attenuates the flow impingement zone at the neck of bifurcation-type aneurysms, which leads to decreased hemodynamic stress.1 Nyberg et al.16 reported a case series in which stent reconstruction alone created favorable hemodynamic changes, enabling aneurysmal shrinkage over time. In simple coiling without stenting, as Ishii et al.11 reported, no angular remodeling occurred secondary to the straightening effect. The porosity of neck-bridging stents is not as low as that of flow-diverting stents and is insufficient to directly decrease flow into the aneurysm.17,18 However, progressive delayed thrombosis is known to occur after deployment of neck-bridging stents secondary to a delayed flow-diversion effect, most probably caused by the effect of straightening the parent vessels.11 In our study, neck diameters and VER were not significantly different in progressive thrombosis patients. However, parent vessel angle change immediately after the procedure in the progressive thrombosis group tended to be larger than that in the no thrombosis group. Furthermore, there was a significant difference in results at the 6-month follow-up. In logistic regression analysis of aneurysm neck diameter and parent vessel angle change immediately after the procedure, results were not significant, but in univariate analysis they tended toward significance. Therefore, these factors may be useful intraoperative factors related to progressive thrombosis. However, although there was no significant difference for aneurysm neck diameter, there was a tendency toward significance for parent vessel angle change. Outcomes after SAC for AcomA aneurysms were good, and they showed that hemodynamic changes over time
WORLD NEUROSURGERY -: e1-e7, - 2019
Evaluating Effects of Straightening Parent Vessels We based our evaluation of the effects of straightening the parent vessels on hemodynamic changes in the findings from CFD studies; however, CFD studies are not widely used clinically. Ishii et al.11 correlated the effects of straightening the parent vessels with decreased recanalization in stent-assisted coil embolization. The authors found that although VER was not significantly different for decreased recanalization when comparing stentassisted coiling versus coiling alone, they did see a significant difference in parent vessel angle change, which was measured on the working projections of the DSA images. Those authors also evaluated intracranial unruptured aneurysms with a diameter 7 mm and found that aneurysms with an angular change >20 were less likely to recanalize. In our study, evaluated aneurysms were limited to those on the AcomA because those vessels, which are not fixed by osseous structures and have characteristics such as small diameters and thin vessel walls, are more mobile. Therefore, the effect of straightening the parent vessels is greater than for immobile vessels such as the internal carotid artery. Furthermore, because the AcomA can be 3-dimensionally mobile, we measure parent vessel angles using the 3-dimensional DSA data. However, interobserver and intraobserver measurement errors should be considered with this method. Thus, future studies with higher numbers of patients and more accurate measurement methods are required. Limitations In our study, statistical analyses of the effects of stent placement were insufficient because there was no control group with which to compare results. Although the comparisons between simple coil embolization and stent-assisted coil embolization, or between mobile vessels and immobile vessels such as the internal carotid artery, may be necessary, outcomes are affected by multiple factors such as the structure of the aneurysms and parent vessels, surgical techniques and surgical skill levels, the type of device used, and individual patient characteristics. Also, our patient numbers were too small to enable evaluation of additional multiple factors. Further analyses and accumulation of cases are necessary to prove the effects of parent vessel angle change. Additionally, in this study, nonblinded authors interpreted the radiographic results and angle measurements. We conclude that a decreased recanalization rate and progressive thrombosis are caused by the effects of straightening the parent vessels that result from stent placement. However, the results of our study do not reflect the effect of stent placement itself because the treatment method was combined with coil embolization. For the effect of stent placement alone to be evaluated, a CFD study may be necessary before and
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ORIGINAL ARTICLE YUSUKE FUNAKOSHI ET AL.
STENT-ASSISTED COIL EMBOLIZATION FOR ACOMA ANEURYSMS
after stent placement without coil embolization. Increased numbers of clinical studies using CFD are expected, and we are planning future studies accordingly.
straightening of the parent vessels may be a factor related to treatment outcomes. ACKNOWLEDGEMENT
CONCLUSIONS The outcomes of SAC for AcomA aneurysms are generally good. Furthermore, hemodynamic changes resulting from the
REFERENCES 1. Gao B, Baharoglu M, Malek AM. Angular remodeling in single stent-assist coiling displaces and attenuates the flow impingement zone at the neck of intracranial bifurcation aneurysms. Neurosurgery. 2013;72:739-748. 2. Kono K, Shintani A, Terada T. Hemodynamic effects of stent struts versus straightening of vessels in stent-assisted coil embolization for cerebral sidewall aneurysms. PLoS One. 2014;23: e108033. 3. Geyik S, Yavuz K, Yurttutan N, Saatci I, Cekirge HS. Stent-assisted coiling in endovascular treatment of 500 consecutive cerebral aneurysms with long-term follow-up. AJNR Am J Neuroradiol. 2013;34:2157-2162. 4. Hong Y, Wang YJ, Deng Z, Wu Q, Zhang JM. Stent-assisted coiling versus coiling in the treatment of an intracranial aneurysm: A systematic review and meta-analysis. PLoS One. 2014;9:e82311. 5. Johnson AK, Munich SA, Heiferman DM, Lopes DK. Stent-assisted embolization of 64 anterior communicating artery aneurysms. J Neurointervent Surg. 2013;5:62-65. 6. Piotin M, Blanc R, Spelle L, et al. Stent-assisted coiling of intracranial aneurysms: Clinical and angiographic results in 216 consecutive aneurysms. Stroke. 2010;41:110-115. 7. Gonzalez N, Sedrak M, Martin N, Vinuela F. Impact of anatomic features in the endovascular embolization of 181 anterior communicating artery aneurysms. Stroke. 2008;39:2776-2782. 8. Huang Q, Xu Y, Hong B, Zhao R, Zhao W, Liu J. Stent-assisted embolization of wide-neck anterior
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The authors thank Trent Rogers, Ph.D., and Jane Charbonneau, D.V.M., from the Edanz Group (www.edanzediting.com/ac) for editing a draft of the manuscript for this article.
communicating artery aneurysms: Review of 21 consecutive cases. AJNR Am J Neuroradiol. 2009;30: 1502-1506. 9. Schuette AJ, Hui FK, Spiotta AM, et al. Endovascular therapy of very small aneurysms of the anterior communicating artery: Five-fold increased incidence of rupture. Neurosurgery. 2011;68:731-737. 10. Fang S, Brinjikji W, Murad MH, Kallmes DF, Cloft HJ, Lanzino G. Endovascular treatment of anterior communicating artery aneurysms: A systematic review and meta-analysis. AJNR Am J Neuroradiol. 2014;35:943-947. 11. Ishii A, Chihara H, Kikuchi T, Arai D, Ikeda H, Miyamoto S. Contribution of the straightening effect of the parent artery to decreased recanalization in stent-assisted coiling of large aneurysms. J Neurosurg. 2017;127:1063-1069. 12. Kocur D, Slusarczyk W, Przybyłko N, Ba_zowski P, Właszczuk A, Kwiek S. Stent-assisted endovascular treatment of anterior communicating artery aneurysm: Literature review. Pol J Radiol. 2016;81: 374-379. 13. Huang QH, Wu YF, Shen J, et al. Endovascular treatment of acutely ruptured, wide-necked anterior communicating artery aneurysms using the Enterprise stent. J Clin Neurosci. 2013;20:267-271. 14. Cho Y, Jeon J, Rhim J, et al. Progressive thrombosis of small saccular aneurysms filled with contrast immediately after coil embolization: Analysis of related factors and long-term followup. Neuroradiology. 2015;57:615-623.
Systematic review and meta-analysis. World Neurosurg. 2016;93:271-278. 16. Nyberg EM, Larson TC. Beneficial remodeling of small saccular intracranial aneurysms after staged stent only treatment: A case series. J Stroke Cerebrovasc Dis. 2014;23:80-85. 17. Huang QH, Wu YF, Xu Y, Hong B, Zhang L, Liu JM. Vascular geometry change because of endovascular stent placement for anterior communicating artery aneurysms. AJNR Am J Neuroradiol. 2011;32:1721-1725. 18. Roszelle BN, Gonzalez LF, Babiker MH, Ryan J, Albuquerque FC, Frakes DH. Flow diverter effect on cerebral aneurysm hemodynamics: An in vitro comparison of telescoping stents and the Pipeline. Neuroradiology. 2013;55:751-758.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 2 November 2018; accepted 6 February 2019 Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.02.066 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
15. Feng MT, Wen WL, Feng ZZ, Fang YB, Liu JM, Huang QH. Endovascular embolization of intracranial aneurysms: to use stent(s) or not?
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ORIGINAL ARTICLE YUSUKE FUNAKOSHI ET AL.
STENT-ASSISTED COIL EMBOLIZATION FOR ACOMA ANEURYSMS
SUPPLEMENTARY DATA
Supplemental Table 1. Summary of the 24 Cases with AcomA Aneurysm Treated by SAC Dome Neck Case Age Sex (mm) (mm)
Stent Type
VER
Preoperative Postoperative 6-Month Initial 6-Month Angle ( ) Angle ( ) Angle ( ) DSA DSA
1
57
M
7.03
3.53
Enterprise
39.5
98.7
151.6
NR
2
56
M
7.46
4.06
Enterprise
17.56
3
67
F
3.43
2.7
Enterprise
32.76
100.8
135
155.2
107.6
121.1
158.4
4
48
M
8.02
5.23
Enterprise
5
58
M
7.08
4.28
Neuroform EZ
24.61
101.8
135.8
27.75
110.1
141.9
6
48
M
7.06
3.85
Neuroform EZ
37.25
78.1
119.6
7
68
F
28.94 11.49
Neuroform EZ
7.6
99
106.1
8
68
M
10.27
8.84
Neuroform EZ
17.03
109.1
110.6
9
63
M
4.96
3.8
Neuroform EZ
17.18
92.4
116.1
10
55
M
6.98
4.86
Enterprise
33.7
64,8
141.3
11
70
M
6.69
5.09
Enterprise
34.46
102.5
12
55
M
11.81
4.93
Enterprise
20.74
13
67
F
5.8
3.11
Neuroform EZ
27.19
14
79
M
7.55
5.1
Neuroform EZ
15
70
M
7.44
5.68
16
50
F
7
4.41
17
54
M
7.47
3.67
18
75
F
10.29
19
81
F
5.5
3.81 Neuroform Altas 34.84
20
52
F
7.77
5.03
LVIS Jr
21
57
M
7.99
7.15
LVIS Jr
22
77
F
4.69
4.56 Neuroform Altas 31.2
23
63
M
8.54
7.09 Neuroform Altas 23.36
24
63
F
6.99
5.23
mRS Follow-up (Pre, Last) (Month)
CO
Asymptomatic TE
0, 0
84
NR
CO
Asymptomatic TE
0, 0
74
NR
NR
0, 0
17
160.3
NR
NR
0, 0
14
151.9
DF
NR
0, 0
49
159
DF
CO
0, 0
18
130.6
DF
NR
Asymptomatic TE
0, 0
57
147.3
DF
CO
Asymptomatic TE
0, 0
33
149.4
DF
CO
0, 0
52
156.5
DF
CO
0, 0
24
129.2
NA
NR
NA
CI Gastric ulcer
2, 2
13
98.1
128.4
132.8
DF
CO
Asymptomatic TE
0, 0
38
92.4
116.1
149.4
NR
CO
Asymptomatic TE
0, 0
30
22.75
87.9
121.1
140.6
DF
DF
0, 0
36
LVIS Jr
27.69
23.9
94.7
147.7
NR
CO
Asymptomatic TE
0, 0
12
LVIS Jr
36.99
53.1
137.8
161
DF
CO
Symptomatic TE
0, 0
18
LVIS Jr
36.48
52.8
76.2
98.9
NR
CO
0, 0
14
7.86 Neuroform Altas 17.43
61.6
81.6
NA
DF
NA
Asymptomatic TE Disuse syndrome
1, 4
1
84
94.7
94.8
NR
CO
Asymptomatic TE
0, 0
10
24.12
117.8
142.6
151.3
NR
NR
0, 0
6
21.79
116.8
133.9
149.7
DF
NR
Asymptomatic TE
0, 0
6
134
135.8
137
NR
NR
Asymptomatic TE
0, 0
6
95
99.6
117.2
DF
NR
Asymptomatic TE
0, 0
6
88.3
131.7
154.5
NR
CO
0, 0
6
LVIS Jr
132.3
Complication
33.77
VER, volume embolization ratio; DSA, digital subtraction angiography; mRS, modified Rankin Scale; M, male; NR, neck-remnant; CO, complete-obliteration; DF, dome-filling; TE, thromboembolism; F, female; CI, cerebral infarction; SAC, stent-assisted coil embolization; AcomA, anterior communicating artery.
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Effect of Straightening the Parent Vessels in Stent-Assisted Coil Embolization for Anterior Communicating Artery Aneurysms Yusuke Funakoshi1, Hirotoshi Imamura1, Shoichi Tani1, Hidemitsu Adachi1, Ryu Fukumitsu1, Tadashi Sunohara1, Keita Suzuki1, Yoshihiro Omura1, Yuichi Matsui1, Natsuhi Sasaki1, Toshiaki Bando2, Tatsumaru Fukuda1, Ryo Akiyama1, Kazufumi Horiuchi1, Shinji Kajiura1, Masashi Shigeyasu1, Nobuyuki Sakai1
BACKGROUND: Stent-assisted coil embolization (SAC) for treating anterior communicating artery (AcomA) aneurysms is safe and effective. Straightening of parent vessels by stent placement can lead to progressive thrombosis. We describe our experience with SAC for AcomA aneurysms and demonstrate the effect of straightening the parent vessels.
-
METHODS: A total of 26 patients with AcomA aneurysms were treated using SAC in our institute between July 2010 and December 2017. Follow-up digital subtraction angiography was performed 6 months after treatment, magnetic resonance angiography was performed every year, and outcomes were analyzed.
was significant at the 6-month follow-up. The median followup term was 18 months. No patients required retreatment. CONCLUSIONS: Good SAC outcomes were achieved for AcomA aneurysms, and hemodynamic changes related to straightening of the parent vessels is a consideration in SAC.
-
-
RESULTS: From all aneurysms (n [ 24), 12 (50.0%) were neck remnant, and 12 (50.0%) were dome-filling types immediately after the procedure. At the 6-month digital subtraction angiography follow-up (n [ 22), 13 (59.1%) aneurysms were complete obliteration, 8 (36.4%) were neck remnant, and 1 (4.5%) was dome filling. The median parent vessel angle was measured preoperatively at 98.1 , increased to 124.8 immediately after stent deployment, and further increased to 149.6 at the 6-month follow-up. Progressive thrombosis was observed in 13 of 22 (59.1%) aneurysms. The parent vessel angle change immediately after stent deployment in the progressive thrombosis group tended to be larger than that observed in the no thrombosis group; this change
-
Key words Aneurysmal stenting - Anterior communicating artery - Progressive thrombosis - Stent-assisted coil embolization - Straightening of parent vessels -
Abbreviations and Acronyms AcomA: Anterior communicating artery CFD: Computational fluid dynamics CO: Complete obliteration DF: Dome filling DSA: Digital subtraction angiography MRA: Magnetic resonance angiography mRS: Modified Rankin Scale
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INTRODUCTION
S
tent-assisted coil embolization (SAC) is a preferred technique in the treatment of wide-neck intracranial aneurysms. Stent-assisted techniques make it possible to preserve the parent vessels and perform sufficient coil embolization of aneurysms, which are technically difficult to treat. Furthermore, straightening of the parent vessels and the stent strut itself have been shown to alter hemodynamics in both bifurcation-type1 and sidewall-type aneurysms,2 based on computational fluid dynamics (CFD) studies. Neck-bridging stents have been widely indicated for wide-neck intracranial aneurysms, and SAC has provided higher rates of complete occlusion and low rates of recanalization in longterm follow-up studies compared with coiling alone.3-6 Anterior communicating artery (AcomA) aneurysms have anatomic features that differ from internal carotid artery aneurysms. In the past, AcomA aneurysms were difficult to treat with coil embolization because endovascular treatment was limited by the typically small diameter and acute angles of the parent
NR: Neck remnant SAC: Stent-assisted coil embolization VER: Volume embolization ratio From the 1Department of Neurosurgery, Kobe City Medical Center General Hospital, Kobe City; and 2Department of Neurosurgery and Stroke Center, Shinko Hospital, Kobe City, Japan To whom correspondence should be addressed: Yusuke Funakoshi, M.D. [E-mail: [email protected]] Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.02.066 Journal homepage: www.journals.elsevier.com/world-neurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
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ORIGINAL ARTICLE YUSUKE FUNAKOSHI ET AL.
STENT-ASSISTED COIL EMBOLIZATION FOR ACOMA ANEURYSMS
vessels.7-9 However, such aneurysms have been rendered treatable by the development of endovascular techniques and devices such as newer microguidewires or catheters and by balloon-assisted or stent-assisted coiling.3,5,10 Recently, stent-assisted coil embolization for AcomA aneurysms has been widely indicated, and the effect of straightening the parent vessels and the resulting hemodynamic changes mediated by stent placement have been a research focus.11 AcomA complexes can be mobilized by stent placement because the complexes are not fixed to osseous structures and they have characteristics such as small diameters and thin vessel walls. Data are insufficient to determine the ramifications of the effect of straightening a parent vessel in SAC for AcomA aneurysms. Although a CFD study may be necessary for full evaluation, CFD study has been used in only a few clinical cases. In this report, we describe our experience using SAC for AcomA aneurysms and describe the effect of straightening the parent vessels, based on parent vessel angle changes.
Table 1. Patient Characteristics (N ¼ 24) Age (years)
63 (55e70)
Sex Female
9 (37.5%)
Male
15 (62.5%)
Background Smoke
13 (54.2%)
HT
13 (54.2%)
DL
7 (29.2%)
DM
2 (8.4%)
Aneurysm dome (mm)
7.3 (6.8e8.0)
Aneurysm neck (mm)
4.9 (3.8e5.6)
Ruptured aneurysm
1 (4.2%)
Median (interquartile range). HT, hypertension; DL, dyslipidemia; DM, diabetes mellitus.
MATERIALS AND METHODS Characteristics of Patients and Aneurysms A total of 24 consecutive patients (9 women and 15 men) with AcomA aneurysms were treated in our institute using SAC between July 2010 and December 2017. We excluded all patients undergoing repeated aneurysmal therapy. Indications for SAC included aneurysm neck size >4 mm, unfavorable dome-to-neck ratio <2, coil instability, or a decision by the senior neurosurgeon that simple coiling, balloon-assisted techniques, or the double-catheter technique were inadequate treatment approaches. Patients’ characteristics are summarized in Table 1. The median patient age was 63 years; 13 patients (54.2%) were smokers, and 13 (54.2%) had previously received diagnoses of hypertension. The median aneurysm dome diameter was 7.3 mm, and the median aneurysm neck diameter was 4.9 mm. The study contained 1 (4.2%) patient with a previously ruptured aneurysm.
Since 2015 we have most often used a hybrid braided closed-cell stent, LVIS Jr. (MicroVention-Terumo, Tustin, California, USA) as a successor to the Neuroform EZ stent. The Neuroform Atlas (Stryker Neurovascular, Fremont, California, USA) is now used to treat aneurysms in small parent vessels with acute angles. Coiling was performed immediately after stent deployment through the microcatheter, which either was placed inside the aneurysm before stent deployment and jailed between the stent and the vessel wall (jailing technique) or was advanced through the stent struts after stent deployment (trans-cell technique). The volume embolization ratio
Perioperative Antiplatelet Management Dual antiplatelet therapy with aspirin and clopidogrel is generally performed for SAC in our institute. Patients took 100 mg aspirin and 75 mg clopidogrel daily for at least 7 days before SAC. Antiplatelet activity was assessed using aspirin and P2Y12 assays (VerifyNow; Accumetrics, San Diego, California, USA) the day before the procedure. When aspirin reaction unit measurements were >550, aspirin was increased to 200 mg. When P2Y12 reaction unit measurements were >220, a loading dose of 20 mg prasugrel was given, and prasugrel was decreased to 3.75 mg once per day, the following day. In patients showing no resistance to antiplatelet therapy, clopidogrel was decreased gradually, beginning 6 months after the procedure, and was discontinued after 1 year. Aspirin was continued as a lifelong treatment. Endovascular Procedures All patients received heparin after an arterial puncture, to maintain increased activated clotting time at approximately 300 seconds during the procedure. Initially, open-cell Neuroform EZ (Stryker Neurovascular, Kalamazoo, Michigan, USA) and closed-cell Enterprise (Cordis Neurovascular Inc., Miami, Florida, USA) stents were used.
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Figure 1. Measurement of the angle between 2 lines, which was approximated as a straight line passing through the center of the parent vessels, from 3-dimensional data derived from digital subtraction angiography and y use of Mimics and 3-matic software (Materialize Japan, Yokohama, Japan).
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ORIGINAL ARTICLE YUSUKE FUNAKOSHI ET AL.
STENT-ASSISTED COIL EMBOLIZATION FOR ACOMA ANEURYSMS
(VER) was measured after the procedure, and the parent vessel angles were measured using 3-dimensional data obtained from digital subtraction angiography (DSA) with Mimics and 3-matic software (Materialize Japan, Yokohama, Japan) (Figure 1) before the procedure, immediately afterward, and at the 6-month follow-up (Figure 2).
across the necks of all 24 aneurysms, and the median VER of the aneurysms was 27.4%. Among all aneurysms (n ¼ 24), 12 (50.0%) were NR, and 12 (50.0%) were DF immediately after the procedure. At the 6-month DSA follow-up (n ¼ 22), 13 (59.1%) were CO, 8 (36.4%) were NR, and 1 (4.5%) was DF. No patients required retreatment for recanalization during follow-up. The preoperative median parent vessel angle was 98.1 (n ¼ 24), which increased to 124.8 immediately after stent deployment (n ¼ 24) and further increased to 149.6 at the 6-month follow-up (n ¼ 22). Angle changes immediately after stent deployment with each type of stent are shown in Table 3. The median angle change was 33.6 for the Enterprise stent (n ¼ 7), 23.7 for the Neuroform EZ stent (n ¼ 7), 34.1 for the LVIS Jr. stent (n ¼ 6), and 7.7 for the Neuroform Atlas stent (n ¼ 4). Angle changes after stent deployment for each type of stent were significantly different (P ¼ 0.0417). Factors related to progressive thrombosis are shown in Table 4. Progressive thrombosis was observed in 13 of 22 (59.1%) aneurysms. There was no significant difference in aneurysm dome diameter, aneurysm neck diameter, and VER. The median parent vessel angle change immediately after the procedure in the progressive thrombosis group was 33.6 , which tended to be larger than the 17.1 observed in the no thrombosis group (P ¼ 0.0662). Median angle change at the 6month follow-up in the progressive thrombosis group was significantly larger than that in the no thrombosis group (P ¼ 0.0177). Logistic regression analysis was performed to assess aneurysm neck diameter and parent vessel angle change immediately after the procedure. Results were not significant but tended toward significance in univariate analysis, and both factors may be useful intraoperative factors related to progressive thrombosis (Table 5). Although there was no significant difference for aneurysm neck (P ¼ 0.4062), there was a tendency toward significance for parent vessel angle change (P ¼ 0.0594).
Follow-Up Angiographic results were classified as complete obliteration (CO), neck remnant (NR), and dome filling (DF). Any further filling of the aneurysm sac over time was referred to as recanalization in follow-up DSA or magnetic resonance angiography (MRA). “Progressive thrombosis” meant that aneurysms that were NR or DF immediately after the procedure changed to CO in follow-up DSA. Follow-up DSA was performed 6 months after treatment, and follow-up MRA, using 1.5-T magnet strength, was performed every year. In patients with recanalization, we scheduled retreatment or earlier follow-up DSA. Statistical Analysis Statistical analysis was conducted using JMP software (version 10, SAS Institute, Cary, North Carolina, USA). VER and parent vessel angle changes were analyzed using the Fisher exact test and the Mann-Whitney U test. Results of the logistic regression model were presented as odds ratio, 95% confidence interval, and P value. P < 0.05 was considered statistically significant. RESULTS Embolization Results and Parent Vessel Angle Changes Study outcomes are summarized in Table 2. The median follow-up term was 18 months. Stent wall apposition was verified using conebeam computed tomography. Stents were successfully deployed
Figure 2. 3-dimensional digital subtraction angiographic images showing the parent vessel angles (A, before treatment; B, immediately after treatment; C, 6-month follow-up). Straightening of the parent vessels is
WORLD NEUROSURGERY -: e1-e7, - 2019
visible. White arrowhead, coiled aneurysm; white arrows, distal and proximal stent markers.
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STENT-ASSISTED COIL EMBOLIZATION FOR ACOMA ANEURYSMS
Table 2. Outcomes of DSA After SAC and Factors Related to Recanalization VER (%)
Table 4. Factors Related to Progressive Thrombosis
Factor
Progressive Thrombosis (n [ 13)
No Thrombosis (n [ 9)
P Value
7.0 (6.4e7.5)
7.8 (5.9e8.3)
0.2426
27.4 (21.0e34.3)
Initial DSA outcome (n ¼ 24) CO
0 (0.0%)
Aneurysm dome (mm)
NR
12 (50.0%)
Aneurysm neck (mm)
4.1 (3.7e5.1)
5.1 (4.4e7.1)
0.1089
12 (50.0%)
VER (%)
33.7 (19.2e36.7)
24.1 (22.3e29.5)
0.171
Postoperative angle change ( )
33.6 (23.6e57.1)
17.1 (5.9e32.5)
0.0662
6-month angle change ( )
57.0 (42.2e86.3)
33.5 (26.9e51.8)
0.0177
DF 6-month DSA outcome (n ¼ 22) CO
13 (59.1%)
NR
8 (36.4%)
DF
1 (4.5%) Median (interquartile range). VER, volume embolization ratio.
Parent vessel angle ( ) Preoperative
98.1 (84.0e107.6)
Immediately after
124.8 (107.2e135.6)
6-month follow-up
149.6 (140.0e155.5)
Recanalization
0 (0.0%)
Follow-up (months)
18 (9e41)
Median (interquartile range). DSA, digital subtraction angiography; SAC, stent-assisted coil embolization; VER, volume embolization ratio; CO, complete obliteration; NR, neck remnant; DF, dome filling.
Complications Complications are shown in Table 6. As a procedure-related complication, asymptomatic thromboembolism was observed in 12 patients (50.0%). Although symptomatic thromboembolism was observed in 1 patient (4.2%), this symptom was transient. No aneurysmal ruptures were observed in our study. Complications unrelated to the procedure included hemorrhage from gastric ulcer and hemodynamic cerebral infarction in 1 patient (4.2%). Disuse syndrome caused worsening of the modified Rankin Scale (mRS) in 1 patient (4.2%). At the final follow-up, the mRS was worse in only 1 patient, who had disuse syndrome, and we saw no change in mRS in the remaining patients.
with a high rate of complete angiographic occlusion.10 In this study, the rates of immediate and long-term complete and nearcomplete angiographic occlusion were 88% and 85%. The retreatment rate was 7%, and overall procedure-related morbidity and mortality were 6% and 3%. Endovascular treatment for AcomA aneurysms has developed with a high degree of safety and efficacy. Kocur et al.12 reviewed 3 stent-assisted coil embolizations for AcomA aneurysms and showed that the complete and nearcomplete occlusion rate was 66% to 95% initially and 88% to 95% at follow-up. Johnson et al.5 observed progressive thrombosis at the 6-month follow-up in 17 of 27 (63%) patients with initially incomplete occlusion after SAC for AcomA aneurysms. Because arterial wall reconstruction by stent endothelialization and hemodynamic changes are considered to cause progressive thrombosis,3,6,13 we focused on the effect of straightening the parent vessels as a clinically assessable index. In our study, although the complete angiographic obliteration rate was 0.0% initially, the rate improved to 59.1% at the 6-month follow-up. The median preoperative parent vessel angle was 98.1 , which increased to 124. 8 immediately after stent deployment and further increased to 149.6 at the 6-month follow-up. Progressive thrombosis and parent vessel angle change, and secondary hemodynamic changes can be characteristics of treatment for AcomA aneurysms.
DISCUSSION SAC for AcomA Aneurysms A meta-analysis published in 2014 evaluating coil embolization of AcomA aneurysms showed that coil embolization is associated Table 3. Parent Vessel Straightening Effects for Each Type of Stent Angle Change ( )
P Value
Enterprise (n ¼ 7)
33.6 (26.7e34.2)
0.0417
Neuroform EZ (n ¼ 7)
23.7 (7.1e33.2)
LVIS Jr. (n ¼ 6)
34.1 (21.8e74.3)
Stent Type
Neuroform Atlas (n ¼ 4)
7.7 (2.5e17.7)
Median (interquartile range).
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Progressive Thrombosis Secondary to Straightening Effect of Parent Vessels Cho et al.14 reported that progressive thrombosis is often seen in aneurysms with small neck diameters or high coil packing density
Table 5. Logistic Regression Analysis of Aneurysm Neck Diameter and Parent Vessel Angle Change Immediately After Stent-Assisted Embolization Variable Aneurysm neck (1-mm increments)
Postoperative angle change (1 )
Odds Ratio
95% CI
P Value
0.79
0.37e1.34
0.4062
1.05
0.99e1.14
0.0594
CI, confidence interval.
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STENT-ASSISTED COIL EMBOLIZATION FOR ACOMA ANEURYSMS
Table 6. Complications and Modified Rankin Scale Score After Stent-Assisted Coil Embolization Complication
Number (%)
Procedure-related complication Asymptomatic thromboembolism
12 (50.0)
Symptomatic thromboembolism
1 (4.2)
Aneurysm rupture
0 (0.0)
resulting from the straightening of the parent vessels can be a factor contributing to treatment outcomes, although other factors certainly may be related to aneurysm occlusion. Because progressive thrombosis is expected in AcomA aneurysms treated by SAC, aggressive coil packing is unnecessary. In addition, parent vessel angle changes are significantly different for each type of stent. Although the effect of straightening the parent vessels is higher with closed-cell stents, we should consider that placing these stents is often difficult when the parent vessel angle is too sharp or the parent vessel diameter is too small.
Other complication Gastrointestinal hemorrhage
1 (4.2)
Disuse syndrome
1 (4.2)
Preoperative mRS 0
22 (91.7)
1e2
2 (8.3)
3e5
0 (0.0)
Last mRS 0
22 (91.7)
1e2
1 (4.2)
3e5
1 (4.2)
and in nonbranching aneurysms. SAC also has advantages regarding the progressive thrombosis rate and lower recurrence rate.11,15 A CFD study revealed that angular remodeling by the straightening effect displaces and attenuates the flow impingement zone at the neck of bifurcation-type aneurysms, which leads to decreased hemodynamic stress.1 Nyberg et al.16 reported a case series in which stent reconstruction alone created favorable hemodynamic changes, enabling aneurysmal shrinkage over time. In simple coiling without stenting, as Ishii et al.11 reported, no angular remodeling occurred secondary to the straightening effect. The porosity of neck-bridging stents is not as low as that of flow-diverting stents and is insufficient to directly decrease flow into the aneurysm.17,18 However, progressive delayed thrombosis is known to occur after deployment of neck-bridging stents secondary to a delayed flow-diversion effect, most probably caused by the effect of straightening the parent vessels.11 In our study, neck diameters and VER were not significantly different in progressive thrombosis patients. However, parent vessel angle change immediately after the procedure in the progressive thrombosis group tended to be larger than that in the no thrombosis group. Furthermore, there was a significant difference in results at the 6-month follow-up. In logistic regression analysis of aneurysm neck diameter and parent vessel angle change immediately after the procedure, results were not significant, but in univariate analysis they tended toward significance. Therefore, these factors may be useful intraoperative factors related to progressive thrombosis. However, although there was no significant difference for aneurysm neck diameter, there was a tendency toward significance for parent vessel angle change. Outcomes after SAC for AcomA aneurysms were good, and they showed that hemodynamic changes over time
WORLD NEUROSURGERY -: e1-e7, - 2019
Evaluating Effects of Straightening Parent Vessels We based our evaluation of the effects of straightening the parent vessels on hemodynamic changes in the findings from CFD studies; however, CFD studies are not widely used clinically. Ishii et al.11 correlated the effects of straightening the parent vessels with decreased recanalization in stent-assisted coil embolization. The authors found that although VER was not significantly different for decreased recanalization when comparing stentassisted coiling versus coiling alone, they did see a significant difference in parent vessel angle change, which was measured on the working projections of the DSA images. Those authors also evaluated intracranial unruptured aneurysms with a diameter 7 mm and found that aneurysms with an angular change >20 were less likely to recanalize. In our study, evaluated aneurysms were limited to those on the AcomA because those vessels, which are not fixed by osseous structures and have characteristics such as small diameters and thin vessel walls, are more mobile. Therefore, the effect of straightening the parent vessels is greater than for immobile vessels such as the internal carotid artery. Furthermore, because the AcomA can be 3-dimensionally mobile, we measure parent vessel angles using the 3-dimensional DSA data. However, interobserver and intraobserver measurement errors should be considered with this method. Thus, future studies with higher numbers of patients and more accurate measurement methods are required. Limitations In our study, statistical analyses of the effects of stent placement were insufficient because there was no control group with which to compare results. Although the comparisons between simple coil embolization and stent-assisted coil embolization, or between mobile vessels and immobile vessels such as the internal carotid artery, may be necessary, outcomes are affected by multiple factors such as the structure of the aneurysms and parent vessels, surgical techniques and surgical skill levels, the type of device used, and individual patient characteristics. Also, our patient numbers were too small to enable evaluation of additional multiple factors. Further analyses and accumulation of cases are necessary to prove the effects of parent vessel angle change. Additionally, in this study, nonblinded authors interpreted the radiographic results and angle measurements. We conclude that a decreased recanalization rate and progressive thrombosis are caused by the effects of straightening the parent vessels that result from stent placement. However, the results of our study do not reflect the effect of stent placement itself because the treatment method was combined with coil embolization. For the effect of stent placement alone to be evaluated, a CFD study may be necessary before and
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ORIGINAL ARTICLE YUSUKE FUNAKOSHI ET AL.
STENT-ASSISTED COIL EMBOLIZATION FOR ACOMA ANEURYSMS
after stent placement without coil embolization. Increased numbers of clinical studies using CFD are expected, and we are planning future studies accordingly.
straightening of the parent vessels may be a factor related to treatment outcomes. ACKNOWLEDGEMENT
CONCLUSIONS The outcomes of SAC for AcomA aneurysms are generally good. Furthermore, hemodynamic changes resulting from the
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The authors thank Trent Rogers, Ph.D., and Jane Charbonneau, D.V.M., from the Edanz Group (www.edanzediting.com/ac) for editing a draft of the manuscript for this article.
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Systematic review and meta-analysis. World Neurosurg. 2016;93:271-278. 16. Nyberg EM, Larson TC. Beneficial remodeling of small saccular intracranial aneurysms after staged stent only treatment: A case series. J Stroke Cerebrovasc Dis. 2014;23:80-85. 17. Huang QH, Wu YF, Xu Y, Hong B, Zhang L, Liu JM. Vascular geometry change because of endovascular stent placement for anterior communicating artery aneurysms. AJNR Am J Neuroradiol. 2011;32:1721-1725. 18. Roszelle BN, Gonzalez LF, Babiker MH, Ryan J, Albuquerque FC, Frakes DH. Flow diverter effect on cerebral aneurysm hemodynamics: An in vitro comparison of telescoping stents and the Pipeline. Neuroradiology. 2013;55:751-758.
Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. Received 2 November 2018; accepted 6 February 2019 Citation: World Neurosurg. (2019). https://doi.org/10.1016/j.wneu.2019.02.066 Journal homepage: www.journals.elsevier.com/worldneurosurgery Available online: www.sciencedirect.com 1878-8750/$ - see front matter ª 2019 Elsevier Inc. All rights reserved.
15. Feng MT, Wen WL, Feng ZZ, Fang YB, Liu JM, Huang QH. Endovascular embolization of intracranial aneurysms: to use stent(s) or not?
WORLD NEUROSURGERY, https://doi.org/10.1016/j.wneu.2019.02.066
ORIGINAL ARTICLE YUSUKE FUNAKOSHI ET AL.
STENT-ASSISTED COIL EMBOLIZATION FOR ACOMA ANEURYSMS
SUPPLEMENTARY DATA
Supplemental Table 1. Summary of the 24 Cases with AcomA Aneurysm Treated by SAC Dome Neck Case Age Sex (mm) (mm)
Stent Type
VER
Preoperative Postoperative 6-Month Initial 6-Month Angle ( ) Angle ( ) Angle ( ) DSA DSA
1
57
M
7.03
3.53
Enterprise
39.5
98.7
151.6
NR
2
56
M
7.46
4.06
Enterprise
17.56
3
67
F
3.43
2.7
Enterprise
32.76
100.8
135
155.2
107.6
121.1
158.4
4
48
M
8.02
5.23
Enterprise
5
58
M
7.08
4.28
Neuroform EZ
24.61
101.8
135.8
27.75
110.1
141.9
6
48
M
7.06
3.85
Neuroform EZ
37.25
78.1
119.6
7
68
F
28.94 11.49
Neuroform EZ
7.6
99
106.1
8
68
M
10.27
8.84
Neuroform EZ
17.03
109.1
110.6
9
63
M
4.96
3.8
Neuroform EZ
17.18
92.4
116.1
10
55
M
6.98
4.86
Enterprise
33.7
64,8
141.3
11
70
M
6.69
5.09
Enterprise
34.46
102.5
12
55
M
11.81
4.93
Enterprise
20.74
13
67
F
5.8
3.11
Neuroform EZ
27.19
14
79
M
7.55
5.1
Neuroform EZ
15
70
M
7.44
5.68
16
50
F
7
4.41
17
54
M
7.47
3.67
18
75
F
10.29
19
81
F
5.5
3.81 Neuroform Altas 34.84
20
52
F
7.77
5.03
LVIS Jr
21
57
M
7.99
7.15
LVIS Jr
22
77
F
4.69
4.56 Neuroform Altas 31.2
23
63
M
8.54
7.09 Neuroform Altas 23.36
24
63
F
6.99
5.23
mRS Follow-up (Pre, Last) (Month)
CO
Asymptomatic TE
0, 0
84
NR
CO
Asymptomatic TE
0, 0
74
NR
NR
0, 0
17
160.3
NR
NR
0, 0
14
151.9
DF
NR
0, 0
49
159
DF
CO
0, 0
18
130.6
DF
NR
Asymptomatic TE
0, 0
57
147.3
DF
CO
Asymptomatic TE
0, 0
33
149.4
DF
CO
0, 0
52
156.5
DF
CO
0, 0
24
129.2
NA
NR
NA
CI Gastric ulcer
2, 2
13
98.1
128.4
132.8
DF
CO
Asymptomatic TE
0, 0
38
92.4
116.1
149.4
NR
CO
Asymptomatic TE
0, 0
30
22.75
87.9
121.1
140.6
DF
DF
0, 0
36
LVIS Jr
27.69
23.9
94.7
147.7
NR
CO
Asymptomatic TE
0, 0
12
LVIS Jr
36.99
53.1
137.8
161
DF
CO
Symptomatic TE
0, 0
18
LVIS Jr
36.48
52.8
76.2
98.9
NR
CO
0, 0
14
7.86 Neuroform Altas 17.43
61.6
81.6
NA
DF
NA
Asymptomatic TE Disuse syndrome
1, 4
1
84
94.7
94.8
NR
CO
Asymptomatic TE
0, 0
10
24.12
117.8
142.6
151.3
NR
NR
0, 0
6
21.79
116.8
133.9
149.7
DF
NR
Asymptomatic TE
0, 0
6
134
135.8
137
NR
NR
Asymptomatic TE
0, 0
6
95
99.6
117.2
DF
NR
Asymptomatic TE
0, 0
6
88.3
131.7
154.5
NR
CO
0, 0
6
LVIS Jr
132.3
Complication
33.77
VER, volume embolization ratio; DSA, digital subtraction angiography; mRS, modified Rankin Scale; M, male; NR, neck-remnant; CO, complete-obliteration; DF, dome-filling; TE, thromboembolism; F, female; CI, cerebral infarction; SAC, stent-assisted coil embolization; AcomA, anterior communicating artery.
WORLD NEUROSURGERY -: e1-e7, - 2019
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