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Application of endovascular coiling and subsequent Onyx 34 embolization in anterior communicating artery aneurysms with adjacent hematoma
Accepted Manuscript Title: Application of Endovascular Coiling and Subsequent Onyx 34 Embolization in Anterior Communicating Artery Aneurysms with Adjacent Hematoma Author: Yi-Bin Fang Qiang Li Peng-Fei Yang Qi Zhang Wu Yi-Na Feng Zheng-Zhe Qing-Hai Huang Yi Xu Jian-Min Liu PII: DOI: Reference:
S0303-8467(14)00173-5 http://dx.doi.org/doi:10.1016/j.clineuro.2014.05.007 CLINEU 3716
To appear in:
Clinical Neurology and Neurosurgery
Received date: Revised date: Accepted date:
24-1-2014 13-4-2014 3-5-2014
Please cite this article as: Fang Yi-Bin, Li Qiang, Yang Peng-Fei, Zhang Qi, Yi-Na Wu, Zheng-Zhe Feng, Huang Qing-Hai, Xu Yi, Liu Jian-Min.Application of Endovascular Coiling and Subsequent Onyx 34 Embolization in Anterior Communicating Artery Aneurysms with Adjacent Hematoma.Clinical Neurology and Neurosurgery http://dx.doi.org/10.1016/j.clineuro.2014.05.007 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Application of Endovascular Coiling and Subsequent Onyx 34 Embolization in
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Anterior Communicating Artery Aneurysms with Adjacent Hematoma
Yi-Bin Fang# M.D. ph.D., Qiang Li# M.D. ph.D.,, Peng-Fei Yang M.D. ph.D., Qi Zhang
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M.D. ph.D., Yi-Na Wu M.D., Zheng-Zhe Feng M.D., Qing-Hai Huang M.D. ph.D., Yi
us
Xu* M.D., Jian-Min Liu* M.D.
an
Department of Neurosurgery, Changhai Hospital, Second Military Medical University,
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Shanghai, 200433, P.R. China
Yi-Bin Fang and Qiang Li contributed equally to this work.
*
Yi Xu and Jian-Min Liu are co-corresponding authors.
Ac ce p
te
d
#
* Corresponding author: Yi Xu or Jian-Min Liu Department of Neurosurgery, Changhai hospital, 168 Changhai Road, Shanghai, 200433, P.R. China
E-mail: [email protected] (J. Liu); [email protected] (Y. Xu) Tel: 86-21-31161800 Fax: 86-21-31161800
1
Page 1 of 19
Highlights ► Though limited in scale, this study is encouraging because it demonstrates that combination of coils and Onyx may provide possible benefit in treating ACoA aneurysms
cr
ip t
with high risk of rebleeding. ► Onyx migration into the parent vessel can be a severe complication, and a successful seal test prior to the procedure is helpful to prevent Onyx migration. ► To avoid intra-operative rupture, the Onyx injection should be performed quite slowly. However, with the protection of the balloon, intra-operative rupture can often be handled appropriately.
us
ABSTRACT
Objective Small anterior communicating artery aneurysms with recurrent bleeding and
an
adjacent hematoma may have a high risk of post-operative rebleeding. This clinical study summarizes our preliminary experience with this subset of aneurysms, which were
M
treated with endovascular coiling and subsequent Onyx 34 embolization. Methods We retrospectively reviewed the data of 9 patients suffering from small
d
anterior communicating artery aneurysms treated with the combination of coils and
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reviewed.
te
Onyx. The clinical characteristics, angiographic outcomes, and follow-up results are
Results Endovascular coiling and Onyx embolization were successfully accomplished in all 9 cases. The Raymond scale ratings of the treatments are all class I with the parent arteries kept patent. One patient died of severe brain edema on the 5th post-operative day. The modified Rankin scale (mRS) score for the other 8 patients at follow-ups (6m to 26m, 15.8m on average) was 0 in 5 cases, 1 in 2 cases, and 3 in 1 case. Seven of 8 patients (87.5%) underwent angiographic follow-up that demonstrated persistent durable occlusion with no recanalization.
2
Page 2 of 19
Conclusions Endovascular coiling and subsequent Onyx 34 embolization may be effective in treating anterior communicating artery aneurysms with adjacent hematoma.
safety and efficacy as well as to evaluate the long-term outcome.
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Abbreviations:
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Further studies with larger sample size and adequate follow-up are required to verify its
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ACoA= anterior communicating artery; SAH=subarachnoid hemorrhage;
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mRS=the modified Rankin Scale score.
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Keywords: anterior communicating artery aneurysm; pseudoaneurysm; Onyx;
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1. Introduction
te
d
endovascular treatment
The International Subarachnoid Aneurysm Trial (ISAT) confirmed better outcomes of patients with intracranial aneurysms treated by endovascular coiling than by neurosurgical clipping [1-3]. However, early rebleeding after endovascular coiling is not uncommon [4]. It is reported that the location of an anterior communicating artery (ACoA) aneurysm, presence of an adjacent hematoma, and small aneurysm size are independent risk factors for rebleeding [4]. A possible explanation for the high risk of rebleeding for aneurysms expressing all the risk factors may be the formation of pseudoaneurysms after the rupture of saccular aneurysms [5-7]. This is the technical challenge for endovascular theraphy. We report the successful application of 3
Page 3 of 19
endovascular coiling and subsequent Onyx embolization in 9 cases of small ACoA aneurysms with recurrent bleeding and adjacent hematoma.
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2. Materials and methods The institutional review board of Changhai Hospital, Second Military Medical University
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approved this retrospective study, and the requirement for informed consent was waived.
us
2.1 Patient population
From the aneurysm database between February 2010 and August 2012 in our institution,
an
9 patients with small ACoA aneurysms were identified, all were with adjacent hematoma and treated with a combination of coils and Onyx. Clinical characteristics, procedural
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data, angiographic and follow-up results were reviewed, and are shown in Table 1.
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The studied population included 5 males and 4 females. The age of onset ranged from
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29 to 61 years old (46.4 on average). The pre-operative Hunt and Hess grade was I in 2,
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II in 3, III in 2, and IV in 2 patients. 2.2 Radiographic features
Subarachnoid hemorrhage was confirmed on CT scanning with a Fisher scale of 3 in all patients. Rebleeding was detected clinically in all patients, and formation (n=3) or enlargement (n=6) of hematomas were confirmed by CT scanning prior to the treatment (Tab. 1, Fig. 1). The hematomas were located in the anterior longitudinal fissure or in the frontal lobe, and the volume of the hematoma ranged from 3 mL to 13 mL (6.9 mL on average). The aneurysms were revealed on admission through CT angiography or conventional angiography. The sizes ranged from 2.5 mm to 8.9 mm (3.9 mm on average). The
4
Page 4 of 19
configuration was irregular saccular (Fig. 1) or lobulated (Fig. 2). Moderate to severe
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vasospasm was revealed in 2 cases (Cases 3 and 5).
2.3 Endovascular treatment procedure
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All cases accepted endovascular treatment within 72 hours except one transferred to our
us
center 12 days after onset. The procedures were performed under general anesthesia. A 6-French MPC Envoy guide catheter (Cordis Neurovascular, Miami, FL) was placed
an
in the internal carotid artery (ICA) as distal as possible, and was connected to a double hemostasis valve Y connector. A HyperForm balloon microcatheter (Micro Therapeutics,
M
Irvine, CA) was navigated with its Xpedion guidewire (Micro Therapeutics, Irvine, CA) to the aneurysm neck under road mapping. Then an Echelon-10 (Micro Therapeutics,
te
d
Irvine, CA) microcatheter was navigated with a Transend Platinum 0.014-in microwire (Boston Scientific/Target, Fremont, CA) into the aneurysm. Endovascular coiling was
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performed, and the remodeling technique was used if necessary to obtain a better neck coverage. After the coiling, Onyx 34 was injected with the same microcatheter (Echelon10) under the protection of the Hyperform balloon. Both post-embolization and follow-up angiograms were graded on a 3-point Raymond scale [8].
2.4 Clinical and angiographic follow-up Angiographic follow-ups were performed with conventional angiography, with time intervals scheduled at 3 to 6 months, then again at 12 months. The angiographic results were interpreted independently by 2 authors (YB.F and Q.L.) and were classified
5
Page 5 of 19
according to the Raymond classification. Clinical outcomes at discharge and follow-ups were assessed by the modified Rankin Scale (mRS) score through neurologic examination or a telephone interview.
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3. Results
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3.1 Treatment
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All aneurysms were treated by using endovascular coiling and subsequent Onyx 34 embolization. All procedures were accomplished successfully. One patient with pre-
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operative Hunt-Hess grade IV died of brain edema 5 days after treatment (11%, 1/9, Case 3). The post-operative course was uneventful in the remaining patients.
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3.2 Angiographic results
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Immediate total occlusion was achieved in all cases based on the Raymond
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classification. The parent arteries were kept patent with no Onyx migration into the vessels. Onyx was detected extravasating into the adjacent hematoma in 3 cases. Seven of
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8 surviving patients (87.5%) underwent digital subtraction angiography (DSA) followups at 4 to 12 months (6.7 months on average) that demonstrated persistent durable occlusion with no recanalization. 3.3 Clinical follow-up
The surviving 8 patients were followed up clinically for 6 to 26 months (15.8 months on average). The mRS score was 0 in 5 cases, 1 in 2 cases, and 3 in 1 case. 4. Discussion 4.1 Diagnosis of pseudoaneurysms
6
Page 6 of 19
It is reported that the location on the ACoA [9], presence of an adjacent hematoma, and small aneurysm size [4] are independent risk factors for rebleeding. When all the risk factors are present, the risk of post-operative rebleeding may be quite high. A possible
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explanation may be the formation of pseudoaneurysms after the rupture of saccular
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aneurysms [5-7].
In our series, similar aggravation occurs accompany with the formation or enlargement
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of hematoma， suggesting the possible diagnosis of pseudoaneurysms [10]. On DSA,
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irregular configuration and delayed washout of contrast medium from the aneurysmal sac were detected in all of the aneurysms. Extravasation of the Onyx into the adjacent
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hematoma was detected in 3 cases, which may support the diagnosis of pseudoaneurysms.
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4.2 Prior treatment of pseudoaneurysms
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Treatment for pseudoaneurysms is challenging, and different strategies have been
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previously reported. For patients with distal pseudoaneurysms or patients with proximal lesions who can tolerate a balloon occlusion test, surgical or internal trapping is preferred. Trapping may reduce the risk of post-operative rebleeding, but resultant infarction is inevitable. Sacrifice of the ACoA may not be fatal, but this technique is not always available when the aneurysm is located at the bifurcation of the A1 and ACoA. Furthermore, in particular cases, a permanent visual field defect may be caused by the obliteration of perforating arteries feeding the optic chiasm [11]. Endovascular stenting with or without coiling was reported to be useful in treating pesudoaneurysms with preservation of the parent arteries [12,13]. It is believed that stents can be used to treat aneurysms by changing local hemodynamic status. However,
7
Page 7 of 19
considering the increased risk of rebleeding because of antiplatelet therapy, new approaches should be considered to treat pseudoaneurysms.
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4.3 Application of Onyx in aneurysms The clinical application of Onyx began in 1999 and several studies have been published
cr
about its safety and efficacy in treating side-wall aneurysms [14-16]. Compared with coil
reduced recanalization rates, and lower expense.
us
embolization or stent-assisted coiling, Onyx provides more complete volumetric filling,
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Although complete occlusion of aneurysms with Onyx is feasible by using protective devices, migration of the liquid embolic agent into the parent artery remains a technical
M
challenge. On the other hand, in spite of the high obliteration rate, recanalization is still a challenge, occurring in up to 36% of large and giant aneurysms [14]. This result suggests
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long-term results.
d
that endovascular Onyx packing with balloon assistance may not be adequate for stable
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4.4 Combination of coils and Onyx
Murayama and colleagues compared the benefits of balloons, stents, and coils to prevent Onyx migration, finding that the coils were more effective than the other 2 devices [17]. This result is also supported by Ueno’s research [18]. We performed Onyx embolization under the dual protection of balloon and coils. No Onyx migration into the vessel was detected, suggesting that the coils can be useful to prevent Onyx migration. In addition, the combination of coils and the Onyx increased contact between the aneurysm wall and the coils, allowing Onyx to fill the intra-aneurysmal space more tightly [18]. The combination mimics “steel enhanced concrete”, and could help
8
Page 8 of 19
resistance to flow impulse and to reduce the risk of recanalization [19]. More rapid formation of the intimal layer using a combination of coils and Onyx may also help prevent recurrence [18]. Cekirge and colleagues reported a series of 20 aneurysms treated
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by coils and Onyx with no recurrence in 1-3 years of follow-up [19]. In our series, total
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occlusion was obtained in all cases and remained angiographically stable.
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4.5 Complication prevention
The most important problem during Onyx embolization is prevention of Onyx migration
an
into the vessels. A successful seal test is necessary to avoid Onyx migration. It is helpful to choose a highly compliant balloon such as the Hyperform that provides better neck
M
coverage and causes less intimal injury. When the Onyx injection is finished, the microcatheter should be retracted when the balloon is still inflated. In cases where Onyx
te
prevent distal thrombosis [16].
d
migration does occur, the technique of stent rescue may stabilize the migrated Onyx and
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The formulation of Onyx HD 500 used for embolization of aneurysms differs significantly from the formulations of Onyx 34 or Onyx 18. The higher percentage of EVOH (ethylene vinyl alcohol) in Onyx HD 500 makes it far more viscous and therefore safer to use in aneurysm embolization. In our series, we used Onyx 34 in all 9 cases under the protection of balloon and coils and no Onyx migration was detected in the parent vessels. The post-embolization and follow-up angiogram revealed persistent total occlusion of the aneurysm with no recurrence. We therefore consider it feasible to use Onyx 34 under the dual protection of balloon and coils when Onyx-HD 500 is not available.
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Page 9 of 19
Intra-operative rupture is another lethal complication in Onyx embolization, which can be caused by elevated intra-aneurysmal pressure following Onyx injection. The risk may be much higher in pseudoaneurysms. Extravasation of Onyx into the subarachnoid space
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may be a signal of aneurysm rupture. However, it is sometimes difficult to distinguish the extravasation of Onyx into the subarachnoid space from that into the adjacent hematoma,
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the latter of which can be helpful in preventing rebleeding. It is therefore important to
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determine the boundary of the hematoma before the procedure. When a rupture is suspected, intra-operative Dyna CT is quite useful to resolve the ambiguity. We detected
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Onyx extravasation into the hematoma in 3 cases.
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Because of the protection of the balloon, intra-operative rupture can often be handled appropriately. However, the toxicity of dimethyl sulfoxide (DMSO) in the subarachnoid
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5. Limitations
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space of the brain is a matter of concern.
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Despite the satisfactory result in our series, further evaluation with more patients and longer follow-up is required. It should also be noted that we chose this a strategy for these cases mainly based on the possible diagnosis of pseudoaneurysm, which may sometimes be subjective. 6. Conclusion
Combination of coils and Onyx with the assistance of a Hyperform balloon may provide possible benefit in treating ACoA aneurysms with high risk of rebleeding. Further studies with larger numbers of cases and adequate follow-up are required to verify its safety and efficacy and evaluate its long-term results. Considering the risk of intra-operative rupture
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Page 10 of 19
and Onyx migration, this technique should be applied in carefully evaluated cases with
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high risk of rebleeding.
Conflict of Interest
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The authors have declared no conflict of interest. References
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[1] Molyneux A, Kerr R, Stratton I, Sandercock P, Clarke M, Shrimpton J, et al. International subarachnoid aneurysm trial (isat) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet 2002;360:1267-74.
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[2] Molyneux AJ, Kerr RS, Yu LM, Clarke M, Sneade M, Yarnold JA, et al. International subarachnoid aneurysm trial (isat) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet 2005;366:809-17.
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[3] Molyneux AJ, Kerr RS, Birks J, Ramzi N, Yarnold J, Sneade M, et al. Risk of recurrent subarachnoid haemorrhage, death, or dependence and standardised mortality ratios after clipping or coiling of an intracranial aneurysm in the international subarachnoid aneurysm trial (isat): long-term follow-up. Lancet Neurol 2009;8:427-33. [4] Sluzewski M, van Rooij WJ. Early rebleeding after coiling of ruptured cerebral aneurysms: incidence, morbidity, and risk factors. AJNR Am J Neuroradiol 2005;26:1739-43. [5] Ding H, You C, Yin H. Nontraumatic and noninfectious pseudoaneurysms on the circle of willis: 2 case reports and review of the literature. Surg Neurol 2008;69:4147, 417. [6] Mori K, Kasuga C, Nakao Y, Yamamoto T, Maeda M. Intracranial pseudoaneurysm due to rupture of a saccular aneurysm mimicking a large partially thrombosed aneurysm ("ghost aneurysm"): radiological findings and therapeutic implications in two cases. Neurosurg Rev 2004;27:289-93. [7] Nomura M, Kida S, Uchiyama N, Yamashima T, Yoshikawa J, Yamashita J, et al. Ruptured irregularly shaped aneurysms: pseudoaneurysm formation in a thrombus located at the rupture site. J Neurosurg 2000;93:998-1002.
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[8] Raymond J, Guilbert F, Weill A, Georganos SA, Juravsky L, Lambert A, et al. Long-term angiographic recurrences after selective endovascular treatment of aneurysms with detachable coils. Stroke 2003;34:1398-403.
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[9] Cha KC, Kim JH, Kang HI, Moon BG, Lee SJ, Kim JS. Aneurysmal rebleeding : factors associated with clinical outcome in the rebleeding patients. J Korean Neurosurg Soc 2010;47:119-23.
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[10] Brzozowski K, Frankowska E, Piasecki P, Ziecina P, Zukowski P, BoguslawskaWalecka R. The use of routine imaging data in diagnosis of cerebral pseudoaneurysm prior to angiography. Eur J Radiol 2011;80:e401-9.
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[11] Perlmutter D, Rhoton AJ. Microsurgical anatomy of the anterior cerebral-anterior communicating-recurrent artery complex. J Neurosurg 1976;45:259-72.
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[12] Fiorella D, Albuquerque FC, Deshmukh VR, Woo HH, Rasmussen PA, Masaryk TJ, et al. Endovascular reconstruction with the neuroform stent as monotherapy for the treatment of uncoilable intradural pseudoaneurysms. Neurosurgery 2006;59:291300, 291-300.
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[13] Ahn JY, Cho JH, Jung JY, Lee BH, Yoon PH. Blister-like aneurysms of the supraclinoid internal carotid artery: challenging endovascular treatment with stentassisted coiling. J Clin Neurosci 2008;15:1058-61.
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[14] Cekirge HS, Saatci I, Ozturk MH, Cil B, Arat A, Mawad M, et al. Late angiographic and clinical follow-up results of 100 consecutive aneurysms treated with onyx reconstruction: largest single-center experience. Neuroradiology 2006;48:113-26.
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[15] Molyneux AJ, Cekirge S, Saatci I, Gal G. Cerebral aneurysm multicenter european onyx (cameo) trial: results of a prospective observational study in 20 european centers. AJNR Am J Neuroradiol 2004;25:39-51. [16] Simon SD, Eskioglu E, Reig A, Mericle RA. Endovascular treatment of side wall aneurysms using a liquid embolic agent: a us single-center prospective trial. Neurosurgery 2010;67:855-60, 860. [17] Murayama Y, Vinuela F, Tateshima S, Vinuela FJ, Akiba Y. Endovascular treatment of experimental aneurysms by use of a combination of liquid embolic agents and protective devices. AJNR Am J Neuroradiol 2000;21:1726-35. [18] Ueno J, Tohma N. Endovascular treatment of cerebral aneurysm with coils and onyx. In-vivo experiment. Interv Neuroradiol 2004;10 Suppl 1:51-6. [19] Cekirge HS, Saatci I, Geyik S, Yavuz K, Ozturk H, Pamuk G. Intrasaccular combination of metallic coils and onyx liquid embolic agent for the endovascular treatment of cerebral aneurysms. J Neurosurg 2006;105:706-12.
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Figure Legends Fig. 1. Case 1 (A) Axial CT scan at onset showing subarachnoid hemorrhage. (B) CT scan at presentation in our center showing a new derived hematoma. (C) Left internal
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carotid artery angiogram showing an irregular-bordered ACoA aneurysm.
Fig. 2. Case 1 (A) Immediate image after the coiling of the aneurysm with a Hydrosoft
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2/6. (B) Extravasation of Onyx 34 into the adjacent hematoma. (C), (D) total occlusion of
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the aneurysm on post-embolization angiogram. (E), (F) total occlusion of the aneurysm
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with a healing line (arrow) at 6 months’ follow-up.
Fig. 3. Case 5 (A) Left internal carotid artery angiogram showing an ACoA aneurysm with a dilated distal daughter sac and a posterior communicating aneurysm. (B) Image of Hydrosoft 4/10, 3/10, and dilated Hyperform 4/7. (C) Onyx 34 embolization under road map. (D) Immediate result after the treatment, and (E), (F) at 8 months follow-up.
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Table 1
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Figure 1 .
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Figure 2 .
Figure 3 .
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S0303-8467(14)00173-5 http://dx.doi.org/doi:10.1016/j.clineuro.2014.05.007 CLINEU 3716
To appear in:
Clinical Neurology and Neurosurgery
Received date: Revised date: Accepted date:
24-1-2014 13-4-2014 3-5-2014
Please cite this article as: Fang Yi-Bin, Li Qiang, Yang Peng-Fei, Zhang Qi, Yi-Na Wu, Zheng-Zhe Feng, Huang Qing-Hai, Xu Yi, Liu Jian-Min.Application of Endovascular Coiling and Subsequent Onyx 34 Embolization in Anterior Communicating Artery Aneurysms with Adjacent Hematoma.Clinical Neurology and Neurosurgery http://dx.doi.org/10.1016/j.clineuro.2014.05.007 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Application of Endovascular Coiling and Subsequent Onyx 34 Embolization in
ip t
Anterior Communicating Artery Aneurysms with Adjacent Hematoma
Yi-Bin Fang# M.D. ph.D., Qiang Li# M.D. ph.D.,, Peng-Fei Yang M.D. ph.D., Qi Zhang
cr
M.D. ph.D., Yi-Na Wu M.D., Zheng-Zhe Feng M.D., Qing-Hai Huang M.D. ph.D., Yi
us
Xu* M.D., Jian-Min Liu* M.D.
an
Department of Neurosurgery, Changhai Hospital, Second Military Medical University,
M
Shanghai, 200433, P.R. China
Yi-Bin Fang and Qiang Li contributed equally to this work.
*
Yi Xu and Jian-Min Liu are co-corresponding authors.
Ac ce p
te
d
#
* Corresponding author: Yi Xu or Jian-Min Liu Department of Neurosurgery, Changhai hospital, 168 Changhai Road, Shanghai, 200433, P.R. China
E-mail: [email protected] (J. Liu); [email protected] (Y. Xu) Tel: 86-21-31161800 Fax: 86-21-31161800
1
Page 1 of 19
Highlights ► Though limited in scale, this study is encouraging because it demonstrates that combination of coils and Onyx may provide possible benefit in treating ACoA aneurysms
cr
ip t
with high risk of rebleeding. ► Onyx migration into the parent vessel can be a severe complication, and a successful seal test prior to the procedure is helpful to prevent Onyx migration. ► To avoid intra-operative rupture, the Onyx injection should be performed quite slowly. However, with the protection of the balloon, intra-operative rupture can often be handled appropriately.
us
ABSTRACT
Objective Small anterior communicating artery aneurysms with recurrent bleeding and
an
adjacent hematoma may have a high risk of post-operative rebleeding. This clinical study summarizes our preliminary experience with this subset of aneurysms, which were
M
treated with endovascular coiling and subsequent Onyx 34 embolization. Methods We retrospectively reviewed the data of 9 patients suffering from small
d
anterior communicating artery aneurysms treated with the combination of coils and
Ac ce p
reviewed.
te
Onyx. The clinical characteristics, angiographic outcomes, and follow-up results are
Results Endovascular coiling and Onyx embolization were successfully accomplished in all 9 cases. The Raymond scale ratings of the treatments are all class I with the parent arteries kept patent. One patient died of severe brain edema on the 5th post-operative day. The modified Rankin scale (mRS) score for the other 8 patients at follow-ups (6m to 26m, 15.8m on average) was 0 in 5 cases, 1 in 2 cases, and 3 in 1 case. Seven of 8 patients (87.5%) underwent angiographic follow-up that demonstrated persistent durable occlusion with no recanalization.
2
Page 2 of 19
Conclusions Endovascular coiling and subsequent Onyx 34 embolization may be effective in treating anterior communicating artery aneurysms with adjacent hematoma.
safety and efficacy as well as to evaluate the long-term outcome.
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Abbreviations:
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Further studies with larger sample size and adequate follow-up are required to verify its
us
ACoA= anterior communicating artery; SAH=subarachnoid hemorrhage;
an
mRS=the modified Rankin Scale score.
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Keywords: anterior communicating artery aneurysm; pseudoaneurysm; Onyx;
Ac ce p
1. Introduction
te
d
endovascular treatment
The International Subarachnoid Aneurysm Trial (ISAT) confirmed better outcomes of patients with intracranial aneurysms treated by endovascular coiling than by neurosurgical clipping [1-3]. However, early rebleeding after endovascular coiling is not uncommon [4]. It is reported that the location of an anterior communicating artery (ACoA) aneurysm, presence of an adjacent hematoma, and small aneurysm size are independent risk factors for rebleeding [4]. A possible explanation for the high risk of rebleeding for aneurysms expressing all the risk factors may be the formation of pseudoaneurysms after the rupture of saccular aneurysms [5-7]. This is the technical challenge for endovascular theraphy. We report the successful application of 3
Page 3 of 19
endovascular coiling and subsequent Onyx embolization in 9 cases of small ACoA aneurysms with recurrent bleeding and adjacent hematoma.
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2. Materials and methods The institutional review board of Changhai Hospital, Second Military Medical University
cr
approved this retrospective study, and the requirement for informed consent was waived.
us
2.1 Patient population
From the aneurysm database between February 2010 and August 2012 in our institution,
an
9 patients with small ACoA aneurysms were identified, all were with adjacent hematoma and treated with a combination of coils and Onyx. Clinical characteristics, procedural
M
data, angiographic and follow-up results were reviewed, and are shown in Table 1.
d
The studied population included 5 males and 4 females. The age of onset ranged from
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29 to 61 years old (46.4 on average). The pre-operative Hunt and Hess grade was I in 2,
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II in 3, III in 2, and IV in 2 patients. 2.2 Radiographic features
Subarachnoid hemorrhage was confirmed on CT scanning with a Fisher scale of 3 in all patients. Rebleeding was detected clinically in all patients, and formation (n=3) or enlargement (n=6) of hematomas were confirmed by CT scanning prior to the treatment (Tab. 1, Fig. 1). The hematomas were located in the anterior longitudinal fissure or in the frontal lobe, and the volume of the hematoma ranged from 3 mL to 13 mL (6.9 mL on average). The aneurysms were revealed on admission through CT angiography or conventional angiography. The sizes ranged from 2.5 mm to 8.9 mm (3.9 mm on average). The
4
Page 4 of 19
configuration was irregular saccular (Fig. 1) or lobulated (Fig. 2). Moderate to severe
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vasospasm was revealed in 2 cases (Cases 3 and 5).
2.3 Endovascular treatment procedure
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All cases accepted endovascular treatment within 72 hours except one transferred to our
us
center 12 days after onset. The procedures were performed under general anesthesia. A 6-French MPC Envoy guide catheter (Cordis Neurovascular, Miami, FL) was placed
an
in the internal carotid artery (ICA) as distal as possible, and was connected to a double hemostasis valve Y connector. A HyperForm balloon microcatheter (Micro Therapeutics,
M
Irvine, CA) was navigated with its Xpedion guidewire (Micro Therapeutics, Irvine, CA) to the aneurysm neck under road mapping. Then an Echelon-10 (Micro Therapeutics,
te
d
Irvine, CA) microcatheter was navigated with a Transend Platinum 0.014-in microwire (Boston Scientific/Target, Fremont, CA) into the aneurysm. Endovascular coiling was
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performed, and the remodeling technique was used if necessary to obtain a better neck coverage. After the coiling, Onyx 34 was injected with the same microcatheter (Echelon10) under the protection of the Hyperform balloon. Both post-embolization and follow-up angiograms were graded on a 3-point Raymond scale [8].
2.4 Clinical and angiographic follow-up Angiographic follow-ups were performed with conventional angiography, with time intervals scheduled at 3 to 6 months, then again at 12 months. The angiographic results were interpreted independently by 2 authors (YB.F and Q.L.) and were classified
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according to the Raymond classification. Clinical outcomes at discharge and follow-ups were assessed by the modified Rankin Scale (mRS) score through neurologic examination or a telephone interview.
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3. Results
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3.1 Treatment
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All aneurysms were treated by using endovascular coiling and subsequent Onyx 34 embolization. All procedures were accomplished successfully. One patient with pre-
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operative Hunt-Hess grade IV died of brain edema 5 days after treatment (11%, 1/9, Case 3). The post-operative course was uneventful in the remaining patients.
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3.2 Angiographic results
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Immediate total occlusion was achieved in all cases based on the Raymond
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classification. The parent arteries were kept patent with no Onyx migration into the vessels. Onyx was detected extravasating into the adjacent hematoma in 3 cases. Seven of
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8 surviving patients (87.5%) underwent digital subtraction angiography (DSA) followups at 4 to 12 months (6.7 months on average) that demonstrated persistent durable occlusion with no recanalization. 3.3 Clinical follow-up
The surviving 8 patients were followed up clinically for 6 to 26 months (15.8 months on average). The mRS score was 0 in 5 cases, 1 in 2 cases, and 3 in 1 case. 4. Discussion 4.1 Diagnosis of pseudoaneurysms
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It is reported that the location on the ACoA [9], presence of an adjacent hematoma, and small aneurysm size [4] are independent risk factors for rebleeding. When all the risk factors are present, the risk of post-operative rebleeding may be quite high. A possible
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explanation may be the formation of pseudoaneurysms after the rupture of saccular
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aneurysms [5-7].
In our series, similar aggravation occurs accompany with the formation or enlargement
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of hematoma， suggesting the possible diagnosis of pseudoaneurysms [10]. On DSA,
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irregular configuration and delayed washout of contrast medium from the aneurysmal sac were detected in all of the aneurysms. Extravasation of the Onyx into the adjacent
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hematoma was detected in 3 cases, which may support the diagnosis of pseudoaneurysms.
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4.2 Prior treatment of pseudoaneurysms
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Treatment for pseudoaneurysms is challenging, and different strategies have been
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previously reported. For patients with distal pseudoaneurysms or patients with proximal lesions who can tolerate a balloon occlusion test, surgical or internal trapping is preferred. Trapping may reduce the risk of post-operative rebleeding, but resultant infarction is inevitable. Sacrifice of the ACoA may not be fatal, but this technique is not always available when the aneurysm is located at the bifurcation of the A1 and ACoA. Furthermore, in particular cases, a permanent visual field defect may be caused by the obliteration of perforating arteries feeding the optic chiasm [11]. Endovascular stenting with or without coiling was reported to be useful in treating pesudoaneurysms with preservation of the parent arteries [12,13]. It is believed that stents can be used to treat aneurysms by changing local hemodynamic status. However,
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considering the increased risk of rebleeding because of antiplatelet therapy, new approaches should be considered to treat pseudoaneurysms.
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4.3 Application of Onyx in aneurysms The clinical application of Onyx began in 1999 and several studies have been published
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about its safety and efficacy in treating side-wall aneurysms [14-16]. Compared with coil
reduced recanalization rates, and lower expense.
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embolization or stent-assisted coiling, Onyx provides more complete volumetric filling,
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Although complete occlusion of aneurysms with Onyx is feasible by using protective devices, migration of the liquid embolic agent into the parent artery remains a technical
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challenge. On the other hand, in spite of the high obliteration rate, recanalization is still a challenge, occurring in up to 36% of large and giant aneurysms [14]. This result suggests
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long-term results.
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that endovascular Onyx packing with balloon assistance may not be adequate for stable
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4.4 Combination of coils and Onyx
Murayama and colleagues compared the benefits of balloons, stents, and coils to prevent Onyx migration, finding that the coils were more effective than the other 2 devices [17]. This result is also supported by Ueno’s research [18]. We performed Onyx embolization under the dual protection of balloon and coils. No Onyx migration into the vessel was detected, suggesting that the coils can be useful to prevent Onyx migration. In addition, the combination of coils and the Onyx increased contact between the aneurysm wall and the coils, allowing Onyx to fill the intra-aneurysmal space more tightly [18]. The combination mimics “steel enhanced concrete”, and could help
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resistance to flow impulse and to reduce the risk of recanalization [19]. More rapid formation of the intimal layer using a combination of coils and Onyx may also help prevent recurrence [18]. Cekirge and colleagues reported a series of 20 aneurysms treated
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by coils and Onyx with no recurrence in 1-3 years of follow-up [19]. In our series, total
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occlusion was obtained in all cases and remained angiographically stable.
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4.5 Complication prevention
The most important problem during Onyx embolization is prevention of Onyx migration
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into the vessels. A successful seal test is necessary to avoid Onyx migration. It is helpful to choose a highly compliant balloon such as the Hyperform that provides better neck
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coverage and causes less intimal injury. When the Onyx injection is finished, the microcatheter should be retracted when the balloon is still inflated. In cases where Onyx
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prevent distal thrombosis [16].
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migration does occur, the technique of stent rescue may stabilize the migrated Onyx and
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The formulation of Onyx HD 500 used for embolization of aneurysms differs significantly from the formulations of Onyx 34 or Onyx 18. The higher percentage of EVOH (ethylene vinyl alcohol) in Onyx HD 500 makes it far more viscous and therefore safer to use in aneurysm embolization. In our series, we used Onyx 34 in all 9 cases under the protection of balloon and coils and no Onyx migration was detected in the parent vessels. The post-embolization and follow-up angiogram revealed persistent total occlusion of the aneurysm with no recurrence. We therefore consider it feasible to use Onyx 34 under the dual protection of balloon and coils when Onyx-HD 500 is not available.
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Intra-operative rupture is another lethal complication in Onyx embolization, which can be caused by elevated intra-aneurysmal pressure following Onyx injection. The risk may be much higher in pseudoaneurysms. Extravasation of Onyx into the subarachnoid space
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may be a signal of aneurysm rupture. However, it is sometimes difficult to distinguish the extravasation of Onyx into the subarachnoid space from that into the adjacent hematoma,
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the latter of which can be helpful in preventing rebleeding. It is therefore important to
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determine the boundary of the hematoma before the procedure. When a rupture is suspected, intra-operative Dyna CT is quite useful to resolve the ambiguity. We detected
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Onyx extravasation into the hematoma in 3 cases.
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Because of the protection of the balloon, intra-operative rupture can often be handled appropriately. However, the toxicity of dimethyl sulfoxide (DMSO) in the subarachnoid
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5. Limitations
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space of the brain is a matter of concern.
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Despite the satisfactory result in our series, further evaluation with more patients and longer follow-up is required. It should also be noted that we chose this a strategy for these cases mainly based on the possible diagnosis of pseudoaneurysm, which may sometimes be subjective. 6. Conclusion
Combination of coils and Onyx with the assistance of a Hyperform balloon may provide possible benefit in treating ACoA aneurysms with high risk of rebleeding. Further studies with larger numbers of cases and adequate follow-up are required to verify its safety and efficacy and evaluate its long-term results. Considering the risk of intra-operative rupture
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and Onyx migration, this technique should be applied in carefully evaluated cases with
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high risk of rebleeding.
Conflict of Interest
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The authors have declared no conflict of interest. References
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[1] Molyneux A, Kerr R, Stratton I, Sandercock P, Clarke M, Shrimpton J, et al. International subarachnoid aneurysm trial (isat) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet 2002;360:1267-74.
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[2] Molyneux AJ, Kerr RS, Yu LM, Clarke M, Sneade M, Yarnold JA, et al. International subarachnoid aneurysm trial (isat) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet 2005;366:809-17.
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[3] Molyneux AJ, Kerr RS, Birks J, Ramzi N, Yarnold J, Sneade M, et al. Risk of recurrent subarachnoid haemorrhage, death, or dependence and standardised mortality ratios after clipping or coiling of an intracranial aneurysm in the international subarachnoid aneurysm trial (isat): long-term follow-up. Lancet Neurol 2009;8:427-33. [4] Sluzewski M, van Rooij WJ. Early rebleeding after coiling of ruptured cerebral aneurysms: incidence, morbidity, and risk factors. AJNR Am J Neuroradiol 2005;26:1739-43. [5] Ding H, You C, Yin H. Nontraumatic and noninfectious pseudoaneurysms on the circle of willis: 2 case reports and review of the literature. Surg Neurol 2008;69:4147, 417. [6] Mori K, Kasuga C, Nakao Y, Yamamoto T, Maeda M. Intracranial pseudoaneurysm due to rupture of a saccular aneurysm mimicking a large partially thrombosed aneurysm ("ghost aneurysm"): radiological findings and therapeutic implications in two cases. Neurosurg Rev 2004;27:289-93. [7] Nomura M, Kida S, Uchiyama N, Yamashima T, Yoshikawa J, Yamashita J, et al. Ruptured irregularly shaped aneurysms: pseudoaneurysm formation in a thrombus located at the rupture site. J Neurosurg 2000;93:998-1002.
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[8] Raymond J, Guilbert F, Weill A, Georganos SA, Juravsky L, Lambert A, et al. Long-term angiographic recurrences after selective endovascular treatment of aneurysms with detachable coils. Stroke 2003;34:1398-403.
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[9] Cha KC, Kim JH, Kang HI, Moon BG, Lee SJ, Kim JS. Aneurysmal rebleeding : factors associated with clinical outcome in the rebleeding patients. J Korean Neurosurg Soc 2010;47:119-23.
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[10] Brzozowski K, Frankowska E, Piasecki P, Ziecina P, Zukowski P, BoguslawskaWalecka R. The use of routine imaging data in diagnosis of cerebral pseudoaneurysm prior to angiography. Eur J Radiol 2011;80:e401-9.
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[11] Perlmutter D, Rhoton AJ. Microsurgical anatomy of the anterior cerebral-anterior communicating-recurrent artery complex. J Neurosurg 1976;45:259-72.
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[12] Fiorella D, Albuquerque FC, Deshmukh VR, Woo HH, Rasmussen PA, Masaryk TJ, et al. Endovascular reconstruction with the neuroform stent as monotherapy for the treatment of uncoilable intradural pseudoaneurysms. Neurosurgery 2006;59:291300, 291-300.
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[13] Ahn JY, Cho JH, Jung JY, Lee BH, Yoon PH. Blister-like aneurysms of the supraclinoid internal carotid artery: challenging endovascular treatment with stentassisted coiling. J Clin Neurosci 2008;15:1058-61.
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[14] Cekirge HS, Saatci I, Ozturk MH, Cil B, Arat A, Mawad M, et al. Late angiographic and clinical follow-up results of 100 consecutive aneurysms treated with onyx reconstruction: largest single-center experience. Neuroradiology 2006;48:113-26.
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[15] Molyneux AJ, Cekirge S, Saatci I, Gal G. Cerebral aneurysm multicenter european onyx (cameo) trial: results of a prospective observational study in 20 european centers. AJNR Am J Neuroradiol 2004;25:39-51. [16] Simon SD, Eskioglu E, Reig A, Mericle RA. Endovascular treatment of side wall aneurysms using a liquid embolic agent: a us single-center prospective trial. Neurosurgery 2010;67:855-60, 860. [17] Murayama Y, Vinuela F, Tateshima S, Vinuela FJ, Akiba Y. Endovascular treatment of experimental aneurysms by use of a combination of liquid embolic agents and protective devices. AJNR Am J Neuroradiol 2000;21:1726-35. [18] Ueno J, Tohma N. Endovascular treatment of cerebral aneurysm with coils and onyx. In-vivo experiment. Interv Neuroradiol 2004;10 Suppl 1:51-6. [19] Cekirge HS, Saatci I, Geyik S, Yavuz K, Ozturk H, Pamuk G. Intrasaccular combination of metallic coils and onyx liquid embolic agent for the endovascular treatment of cerebral aneurysms. J Neurosurg 2006;105:706-12.
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Figure Legends Fig. 1. Case 1 (A) Axial CT scan at onset showing subarachnoid hemorrhage. (B) CT scan at presentation in our center showing a new derived hematoma. (C) Left internal
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carotid artery angiogram showing an irregular-bordered ACoA aneurysm.
Fig. 2. Case 1 (A) Immediate image after the coiling of the aneurysm with a Hydrosoft
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2/6. (B) Extravasation of Onyx 34 into the adjacent hematoma. (C), (D) total occlusion of
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the aneurysm on post-embolization angiogram. (E), (F) total occlusion of the aneurysm
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with a healing line (arrow) at 6 months’ follow-up.
Fig. 3. Case 5 (A) Left internal carotid artery angiogram showing an ACoA aneurysm with a dilated distal daughter sac and a posterior communicating aneurysm. (B) Image of Hydrosoft 4/10, 3/10, and dilated Hyperform 4/7. (C) Onyx 34 embolization under road map. (D) Immediate result after the treatment, and (E), (F) at 8 months follow-up.
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Table 1
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Figure 2 .
Figure 3 .
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