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Hemorrhagic stroke
Stent-assisted coiling of paraclinoid aneurysms: risks and effectiveness
  1. Christopher S Ogilvy1,3,4,
  2. Sabareesh K Natarajan1,3,
  3. Shady Jahshan1,3,
  4. Yuval Karmon1,3,
  5. Xinyu Yang4,5,
  6. Kenneth V Snyder1,3,
  7. L Nelson Hopkins1,2,3,
  8. Adnan H Siddiqui1,2,3,
  9. Elad I Levy1,2,3
  1. 1Department of Neurosurgery and Toshiba Stroke Research Center, School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York, USA
  2. 2Department of Radiology, School of Medicine and Biomedical Sciences, University at Buffalo, State University of New York, Buffalo, New York, USA
  3. 3Department of Neurosurgery, Millard Fillmore Gates Hospital, Kaleida Health, Buffalo, New York, USA
  4. 4Neurovascular Service, Massachusetts General Hospital, Boston, Massachusetts, USA
  5. 5Department of Neurosurgery, Tianjin Medical University General Hospital, Tianjian, China
  1. Correspondence to Elad I Levy, University at Buffalo Neurosurgery, 3 Gates Circle, Buffalo, NY 14209, USA; elevy{at}ubns.com

Abstract

Background Stent assistance for treatment of wide-based aneurysms is becoming rapidly accepted.

Methods Cases of aneurysms arising in the paraclinoid location of the internal carotid artery treated with intracranial stents and/or bare platinum coils were analyzed retrospectively from our prospectively collected database. We identified 70 aneurysms treated with stent assistance (including one stenting-alone case) and 24 aneurysms treated with coiling alone. Stenting-assisted coiling was achieved either as a one-time treatment or as a two-step maneuver with the stent placed several weeks before coiling, or stent-assisted coiling was used as a second maneuver in aneurysms that recanalized after previous coiling.

Results In aneurysms treated with stent assistance, 60% had ≥95% occlusion at treatment completion, a result comparing favorably with the 54.2% rate of ≥95% occlusion associated with coiling alone. At last follow-up, 60 aneurysms treated with stent assistance had a 66.7% incidence of ≥95% occlusion, with no in-stent stenosis; 75% of patients treated with coiling alone had ≥95% aneurysm occlusion. Thrombus occurred during stent deployment in two patients, one with and one without neurologic sequelae; stent displacement occurred in one patient without neurologic sequelae. At last follow-up, 57 of 62 patients (91.9%) treated with stent-assisted coiling experienced excellent/good outcomes (modified Rankin scale score ≤2). These results compared favorably with those for the coiling-alone group in which 23 of 24 (95.8%) had good outcomes.

Conclusion Stent-assisted coiling of paraclinoid aneurysms did not add significantly to morbidity; overall effectiveness was comparable to that of bare coiling of paraclinoid aneurysms. These results require confirmation by a prospective controlled trial.

  • Aneurysm
  • brain
  • coil
  • endovascular coils
  • internal carotid artery aneurysms
  • intervention
  • intracranial aneurysm
  • intracranial stent
  • paraclinoid aneurysms
  • stent

https://doi.org/10.1136/jnis.2010.002303

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    The use of stents in the assistance of wide-necked or large or giant intracranial aneurysms is becoming rapidly adopted.1 There are several reports of the utility of stenting to assist coiling in a variety of locations throughout the intracranial circulation.2–11 Aneurysms that arise in the paraclinoid location of the internal carotid artery are of particular interest for the use of stent-assisted coiling and comprise a large percentage of cases of stent-assisted coiling reported in the literature. In a series reported by Biondi et al2 21 of 42 aneurysms treated were in the paraclinoid location. Lubicz et al6 used stent-assisted coiling in eight paraclinoid lesions among a total of 14 patients reported.

    The purpose of the current study was to retrospectively review our data to evaluate potential risks and overall effectiveness of self-expanding intracranial stent placement as an adjunct in the treatment of intracranial aneurysms in the paraclinoid location. In this article, paraclinoid aneurysms are defined as those that arise from the carotid artery at or distal to the dural ring and proximal to the posterior communicating artery.

    Methods

    Patients included in this study were treated at the University at Buffalo Millard Fillmore Gates Hospital. All patient data are entered prospectively in a database. Retrospective review of the database for this particular study was approved by the institutional review board at the University at Buffalo. Ninety-one patients with 94 intracranial paraclinoid aneurysms treated between September 2001 and September 2008 were analyzed. All patients except two were treated with intravenous conscious sedation anesthesia and a local anesthetic administered to the groin region. In the two remaining patients, general anesthesia was utilized. All patients were fully anticoagulated for the procedure with intravenous heparin.

    At our hospital, patients scheduled to undergo elective stent or flow-diversion device placement receive aspirin (325 mg by mouth daily) and clopidogrel (75 mg by mouth daily) for a minimum of 4 days before the procedure. Those undergoing stenting on a more urgent basis receive aspirin (650 mg by mouth) and clopidogrel (600 mg by mouth) 4 h before the procedure. If stenting is performed as an emergency bailout maneuver, we administer an intravenous bolus dose of glycoprotein IIb/IIIa inhibitor (180 mg/kg eptifibatide at our institution) and then clopidogrel (600 mg by mouth) and aspirin (650 mg by mouth) immediately after the procedure. Eptifibatide (2 mg/kg/min) is continued as an intravenous drip for 4 h after the procedure to allow the clopidogrel to reach therapeutic levels of platelet inhibition. In the rare case of a patient with an acutely ruptured aneurysm undergoing stent placement, the glycoprotein IIb/IIIa inhibitor can be given after the stent is in place and the first or second coil is in proper position. All patients with a stent or flow-diversion device are placed on clopidogrel (75 mg daily) for 3 months and aspirin (325 mg daily) for life. Patients who do not have stent placement are kept on aspirin for life.

    The type of therapy used was decided at the discretion of the treating physician. Although there were no fixed criteria for treating these aneurysms, the treating physicians used stent assistance if they thought that the aneurysm had a higher risk of recurrence with coiling alone. Twenty-four patients with 24 aneurysms were treated with coiling alone. Stent-assisted coiling was performed either as a single (38 aneurysms in 37 patients) or a staged (31 aneurysms in 29 patients) procedure. Stent-alone therapy was used in one patient (one aneurysm). A total of 14 aneurysms (in 13 patients) were recurrent aneurysms that were previously treated by coiling and were retreated with stent assistance (seven staged, seven single setting—20% of the stent-assistance aneurysm group). Of the patients treated with stent assistance, one patient was treated with a Wingspan stent (Boston Scientific, Natick, Massachusetts, USA). The remaining patients were treated with either Neuroform (n=44) (Boston Scientific) or Enterprise (n=25) (Codman & Shurtleff, Inc. Raynham, Massachusetts, USA) stents. Subarachnoid hemorrhage (SAH) was the presentation in 10 patients (two, coiling only; six, single session stent-assisted coiling; two, staged stent-assisted coiling).

    Angiographic results were reviewed retrospectively to evaluate the exact percentage of aneurysm occlusion immediately after definitive treatment. Follow-up angiographic data were collected prospectively and reviewed retrospectively. The degree of aneurysm occlusion was evaluated and recorded. Complications that occurred were also recorded. In addition, angiographic images (CT angiography, magnetic resonance (MR) angiography or conventional catheter-based angiography) were evaluated for any evidence of in-stent stenosis.

    Clinical evaluation of patients was performed with office visits at intervals that ranged from 1 to 12 months. The modified Rankin scale (mRS) was utilized to evaluate functional status.12

    For statistical analysis, data were calculated by χ2 test. The p value was found by checking the χ2 table. Statistical significance was taken if p<0.05.

    Results

    Overall results for 70 aneurysms treated by stent assistance as well as 24 aneurysms treated by coiling alone in this clinical series are summarized in table 1. There were no men in the coiling group, whereas 14.3% of patients in the stent-assistance group were men (p=0.005). Although the aneurysms in the stent-assistance group had a higher average dome size, wider neck and an unfavorable dome-to-neck ratio, none of these differences were statistically significant. Angiography performed immediately after definitive treatment showed ≥95% occlusion in 54.2% of aneurysms in the coiling-only group and 60% of aneurysms in the stent-assistance group. Both treatment groups had on average >24 months of clinical and radiological follow-up, and 75% of aneurysms in the coiling-only group and 66.7% of aneurysms in the stent-assistance group had ≥95% occlusion at last follow-up. There were no statistically significant differences in duration of follow-up or percentage of patients achieving >95% occlusion of the aneurysm immediately after treatment or at last follow-up. Fourteen aneurysms (10 after stent assistance and four after coiling alone) did not have radiological follow-up, and five patients (all five after stent assistance) did not have clinical follow-up.

    View this table:
    Table 1

    Results of treatment of paraclinoid aneurysms and comparison between aneurysms treated by coiling alone versus stent assistance

    The types and numbers of complications encountered are detailed in table 2. Thrombus within the stent during the coiling procedure occurred in one patient and was treated with intra-arterial thrombolytics. In one patient, the stent became displaced during deployment, without neurologic sequelae. One patient experienced a post-coiling hemorrhage that resulted in a poor outcome. This patient was initially treated with endovascular coiling after SAH. After a subsequent SAH from the aneurysm, the patient was retreated with stent-assisted coiling. Although the aneurysm was obliterated, the patient remained in poor clinical condition.

    View this table:
    Table 2

    Complication analysis

    The overall functional outcome of patients treated in this series is summarized in table 3. As can be seen, the majority of patients had unruptured aneurysms. Follow-up was available for 62 patients treated with stent assistance and all patients treated with coiling alone. Seventy-six of 78 patients with unruptured aneurysms recovered to mRS ≤2 at last follow-up, whereas only four of eight patients with ruptured aneurysms recovered to mRS ≤2. There was no statistically significant difference in the outcomes of patients treated with or without a stent in either the ruptured or unruptured group.

    View this table:
    Table 3

    Clinical outcome evaluated by modified Rankin scale score

    Typical results for stenting and coiling at the same treatment session of a wide-necked aneurysm are shown in figure 1. A case in which the aneurysm was initially treated with stenting followed by delayed coiling of the aneurysm 4 weeks later is shown in figure 2. A case in which the patient was initially treated with coil embolization and had coil compaction at follow-up is shown in figure 3. To manage this, the patient was treated with stent placement and subsequent coiling.

    Figure 1
    Figure 1

    Angiographic images illustrating stent placement and coiling performed during the same treatment session in two separate patients. The first is a patient in their mid-50s who was found to have an incidental large left paraclinoid aneurysm (A–C). Preoperatively, the aneurysm projected medially and superiorly (A). After stent deployment and coiling, it was felt that there was near-complete occlusion of the aneurysm (B, C). The second is a patient in their mid-40s with left temporal headaches who was found to have a large left paraclinoid aneurysm (D, E). As can be seen in (D), there is tortuosity of the carotid artery adjacent to the wide-based aneurysm neck. The patient underwent Neuroform stent (Boston Scientific) deployment and coiling that resulted in complete aneurysm occlusion (E).

    Figure 2
    Figure 2

    Angiographic images illustrating stent placement followed by delayed coiling of the aneurysm. The patient is an individual in their mid-60s who presented with a vibration sensation in the head and was found to have a large left paraclinoid aneurysm (A, B). This patient underwent successful stent deployment across the neck of the aneurysm utilizing a 4.5×22 mm Enterprise stent (Cordis) (C) and returned 4 weeks later for coil embolization of the aneurysm. Follow-up angiography 6 months later demonstrated 95% occlusion of the aneurysm, and subsequent coil packing was performed. The patient ultimately had what appeared to be near-complete occlusion of the aneurysm (D, E). The patient did well neurologically with no new neurologic deficits.

    Figure 3
    Figure 3

    Angiographic images illustrating primary coiling of an aneurysm with recanalization followed by stent placement and recoiling. This patient in their mid-40s presented with severe headache and underwent a CT scan that demonstrated a left internal carotid artery aneurysm without subarachnoid hemorrhage. The patient underwent angiography that confirmed the large back-wall paraclinoid aneurysm (A, B). Coil embolization of the lesion with near-complete occlusion of the lesion was performed. Seven months after initial treatment, the patient presented for follow-up angiography, which demonstrated recanalization of the aneurysm (C, D). The lesion was treated with carotid artery Enterprise stent (Cordis) placement and re-coiling of the aneurysm in the same session with ∼95% occlusion of the aneurysm (E, F). A follow-up angiogram 10 months after stent placement and coiling demonstrated a stable lesion with near-complete occlusion of the aneurysm (G, H).

    Discussion

    The tortuosity of the carotid artery as it enters the skull base provides a challenge for both endovascular and surgical management of intracranial aneurysms. In particular, stents may kink or twist as they are deployed in the segment of carotid artery as the vessel leaves the cavernous sinus. Both open-cell and closed-cell stents have been utilized to treat aneurysms in this location.7

    In most series utilizing stent-assisted coiling, a high percentage of lesions are in the paraclinoid location. In the personal series reported by Nelson et al7 eight of 16 patients had paraclinoid lesions. Lubicz et al6 report an initial experience with Enterprise stents in which eight of 14 patients had paraclinoid aneurysms. Biondi et al2 report using Neuroform stents in 42 wide-necked aneurysms, of which 21 of 42 were paraclinoid in location. Similarly, Yavuz et al11 report stent-assisted coiling of aneurysms with Wingspan stents in which 18 of 37 patients harbored paraclinoid aneurysms. Other series in which stents were used in combination with coils report 40%–50% of patients treated having paraclinoid aneurysms.10 13 14 Owing to the high utilization of stent-assisted coiling in the paraclinoid location to date, we have focused on this family of aneurysms for analysis of risks and effectiveness of treatment.

    With respect to thrombotic events, we found that two patients treated with stent-assisted coiling developed thrombus during coiling. One patient suffered neurologically from this event, with decreased vision in the left eye (1.5%). In the second patient, thrombus was noted within the stent during coiling without any obvious neurologic sequelae. Fortunately, this patient was treated under conscious sedation and therefore could be monitored neurologically. Intra-arterial glycoprotein IIb/IIIa platelet inhibitor was administered, and the thrombus resolved without any permanent neurologic sequelae.

    In other series of intracranial stent placement for treatment of aneurysms, the incidence of in-stent stenosis ranges from 4% to 10%.15 16 To date, we have not observed in-stent stenosis as a complicating factor in the management of the patients in our series. Given the retrospective nature of our study and the fact that various imaging modalities including CT, MR and catheter angiography were used to detect in-stent stenosis, these results need to be confirmed by future studies looking specifically for in-stent stenosis in this subset of patients.

    In our series, although the aneurysms that were treated by stent assistance had larger dome size, wider neck and unfavorable dome-to-neck ratios, all these differences were not statistically significant. The decision to use a stent to achieve aneurysm occlusion was based on the treating physician's assessment of the aneurysm–parent vessel morphology and the chance of recurrence after coiling alone. The probable explanation for comparable aneurysm characteristics between aneurysms treated with stent assistance and simple coiling alone could be due to (1) the small number of patients and/or (2) the fact that the numerical indices of dome size, neck size or dome-to-neck ratio do not capture the complexity of aneurysm–parent vessel morphology as perceived by the physician when making the decision to use a stent. As seen in Table 1, there is no statistically significant difference between the percentages of aneurysms that had immediate or follow-up occlusion rates ≥95% in aneurysms treated by stent-assistence and coiling alone.

    Nelson et al7 reviewed 21 articles focusing on stent-supported coil embolization of cerebral aneurysms published between January 1999 and May 2006. They found that the majority of those data reflect use of the Neuroform stent (14 articles, 361 patients). Thirty-five percent of aneurysms were treated after SAH. Approximately 28% of the described aneurysms were large (usually at least 10 mm in diameter). Approximately 7% were giant (uniformly >25 mm). In ∼7.3% of the cases, stent delivery was unsuccessful. Stent malpositioning occurred ∼6.1% of the time overall and in 4.2% of Neuroform cases. No specific malpositioning was reported with Neuroform 2 (Boston Scientific) or Neuroform Treo (Boston Scientific) stents. Approximately 57% of aneurysms were felt to be completely occluded on immediate postprocedure angiography, and 22% were reported to be almost completely occluded. Angiographic follow-up evaluations were reportedly performed in 201 patients (14 articles), with outcome results actually described for 172 patients in 13 articles. The mean time to follow-up angiography was 6.3 months, with a range of 1–18 months. Among those articles in which follow-up outcome was reported, 69% of aneurysms were found at follow-up to be occluded. Thirteen articles reported recanalization data indicating 4.3% of aneurysms occluded on the initial post-treatment angiogram to have recanalized and 14.1% of incompletely occluded aneurysms to have progressive degrees of occlusion. Among the 201 patients with angiographic follow-up, 16 underwent repeat coiling.

    In our series, three different strategies were used to treat paraclinoid aneurysms with a stent and coils. In one approach, patients were initially treated with coiling alone, and after coil compaction occurred, a stent was deployed, followed by further coiling of the aneurysm. These patients were those typically treated initially before the advent of stent therapy. In a second management strategy, a patient was treated up-front with stenting and coiling. This can be done in one of two ways: either the patient can be treated with stents and coils during the same treatment session or a stent can be deployed followed by coil placement several weeks after the stent has been deployed. The decision of which treatment strategy to use was made at the time of initial treatment of the lesion. If arterial access to the lesion was difficult and if stent deployment proceeded smoothly, it was often decided to proceed at the same session with endovascular coiling of the aneurysm. One potential downfall of this strategy would be the increased risk of stent movement during coil placement, given the fact that the stent has not had a chance to heal into the vessel wall or endothelialize. In some cases where the physician thought that it would be difficult to obtain access through the stent tines to coil the aneurysm, a jailed catheter technique (the coiling microcatheter was jailed inside the aneurysm before the stent was deployed) was used. As mentioned above, this decision was also made on a case-wise basis by the treating physician.

    The paraclinoid location of the carotid artery is a challenging arterial structure. The tortuosity of the carotid artery as it crosses the cavernous sinus and enters the intracranial vault is an area where stent deployment may be associated with kinking or twisting of a stent. Given the current radiographic markers of stents, this is extremely difficult to try to analyze radiographically. Although the proximal and distal ends of the stent can be identified, whether the stent is kinked or twisted is difficult to truly ascertain. Luminal diameter of the carotid artery could be assessed; however, this may remain normal on conventional catheter-based angiography with stent twisting or kinking within the vessel. CT angiography could provide better resolution of the stent–parent vessel interface in these cases but was not utilized in all patients in our series. This could account for the absence of in-stent stenosis in our series and needs to be evaluated in the future. Both open-cell (Neuroform) and closed-cell (Enterprise) stents were utilized in this study. We did not notice a significant difference in deployment of coils or ability to coil aneurysms after either type of stent utilization. Certainly, as stent technology evolves, the paraclinoid location will be a major focus for further research in terms of adherence of the stent to the carotid artery through the supraclinoid carotid artery.

    The main limitations of this study are its retrospective nature, which reduces the significance of comparison between aneurysms treated by stent assistance and coiling alone. The modality for follow-up imaging in this series was variable and this imaging was not performed at standard time points, although the average follow-up period was >2 years. There was attrition of patients to follow-up. Parameters that could potentially affect the effectiveness of treatment, such as coil type and packing density, were not recorded. Various modalities were used to assess for in-stent stenosis and aneurysm occlusion, and this assessment was not standardized. Given the turn of the carotid artery in the paraclinoid region and the possibility of more bone artifact at the skull base in these lesions, the assessment of in-stent stenosis may not be precise in this series. Albeit, this is a large series of paraclinoid aneurysms treated with stent assistance (as decided by the treating physician), and the results obtained are comparable to aneurysms treated by simple coiling alone. The significance of this finding needs to be studied in the future in a prospective study of paraclinoid aneurysms that are chosen for stent assistance and randomizing them between coiling alone and stent assistance. This is especially important because stent assistance for aneurysm occlusion is more frequently required for this family of aneurysms than for aneurysm at other locations.

    Conclusions

    To our knowledge, this is the largest series of paraclinoid aneurysm treated by stent assistance reported to date. Results with stent assistance were comparable to those for simple coiling, although the aneurysms chosen for stent assistance probably had complex parent vessel–aneurysm morphology in comparison with aneurysms treated by coiling alone. These findings need to be evaluated prospectively in a controlled trial.

    Key messages

    • Aneurysms that arise in the paraclinoid location of the internal carotid artery are of particular interest for the use of stent-assisted coiling and comprise a large percentage of cases of stent-assisted coiling reported in the literature.

    • The purpose of the current study was to retrospectively review our data to evaluate potential risks and overall effectiveness of self-expanding intracranial stent placement as an adjunct in the treatment of intracranial aneurysms in the paraclinoid location.

    • In this large series of paraclinoid aneurysms treated with stent assistance (as decided by the treating physician), the results obtained were comparable to those for aneurysms treated by simple coiling alone, although the aneurysms chosen for stent assistance probably had complex parent vessel–aneurysm morphology in comparison with aneurysms treated by coiling alone.

    • These findings need to be evaluated prospectively in a controlled trial.

    Acknowledgments

    We thank Paul H. Dressel BFA for preparation of the illustrations and Joyce Davis and Debra J. Zimmer AAS CMA-A for editorial assistance.

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    Footnotes

    • Work conducted at Millard Fillmore Gates Hospital, Kaleida Health, Buffalo, New York, USA

    • Competing interests Dr Hopkins receives research study grants from Abbott (ACT 1 Choice), Boston Scientific (CABANA), Cordis (SAPPHIRE WW) and ev3/Covidien Vascular Therapies (CREATE), and a research grant from Toshiba (for the Toshiba Stroke Research Center); has an ownership/financial interest in AccessClosure, Boston Scientific, Cordis, Micrus and Valor Medical; serves on the Abbott Vascular Speakers' Bureau; receives honoraria from Bard, Boston Scientific, Cordis, and from the following for speaking at conferences: Complete Conference Management, Cleveland Clinic, and SCAI; receives royalties from Cordis (for the AngioGuard device), serves as a consultant to or on the advisory board for Abbott, AccessClosure, Bard, Boston Scientific, Cordis, Gore, Lumen Biomedical, Micrus and Toshiba; and serves as the conference director for Nurcon Conferences/Strategic Medical Seminars LLC. Dr Karmon has received a grant from the American Physicians Fellowship for Medicine in Israel. Dr Levy receives research grant support (principal investigator: Stent-Assisted Recanalization in acute Ischemic Stroke, SARIS), other research support (devices), and honoraria from Boston Scientific and research support from Micrus Endovascular and ev3/Covidien Vascular Therapies; has ownership interests in Intratech Medical Ltd and Mynx/Access Closure; serves as a consultant on the board of Scientific Advisors to Codman & Shurtleff, Inc.; serves as a consultant per project and/or per hour for Micrus Endovascular, ev3/Covidien Vascular Therapies and TheraSyn Sensors, Inc.; and receives fees for carotid stent training from Abbott Vascular and ev3/Covidien Vascular Therapies. Dr Levy receives no consulting salary arrangements. All consulting is per project and/or per hour. Dr Natarajan is the recipient of the 2010–2011 Cushing Award of the Congress of Neurological Surgeons (eligible to receive research support after 1 July 2010). Dr Ogilvy serves as a consultant to Mizuho America. Dr Siddiqui has received research grants from the University at Buffalo and from the National Institutes of Health (NINDS 1R01NS064592-01A1, Hemodynamic induction of pathologic remodeling leading to intracranial aneurysms); is a consultant to Codman & Shurtleff, Inc. Concentric Medical, ev3/Covidien Vascular Therapies and Micrus Endovascular; serves on speakers' bureaus for Codman & Shurtleff, Inc. and Genentech; and has received honoraria from Genentech, Neocure Group LLC, American Association of Neurological Surgeons' courses, and an Emergency Medicine Conference and from Codman & Shurtleff, Inc. for training other neurointerventionists. Dr Siddiqui receives no consulting salary arrangements. All consulting is per project and/or per hour. Dr Jahshan, Dr Snyder and Dr Yang have nothing to disclose.

    • Ethics approval This study was conducted with the approval of the Institutional Review Board at the University at Buffalo.

    • Provenance and peer review Not commissioned; externally peer reviewed.