International Journal of Neuroscience, 2015; Early Online: 1–7 © 2015 Informa Healthcare USA, Inc. ISSN: 0020-7454 print / 1543-5245 online DOI: 10.3109/00207454.2014.992427
ORIGINAL ARTICLE
Treatment of giant/large internal carotid aneurysms: parent artery occlusion or stent-assisted coiling
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Hui Li, Xu-Ying He, Xi-Feng Li, Xin Zhang, Yan-Chao Liu, and Chuan-Zhi Duan Department of Neurosurgery, Neurosurgery Institute, Key Laboratory on Brain Function, Repair and Regeneration of Guangdong, Zhujiang Hospital, Southern Medical University, Guangzhou, China Purpose: Treatment of giant/large internal carotid aneurysm is a challenge for neurologists. Previously, parent artery occlusion was the classic therapy; now the stent-assisted coil embolization has become available in recent years, but the optimal therapy is under debate. The goal of the present study was to compare two endovascular treatment modalities in terms of safety, efficacy and short-term outcomes. Methods: All the patients were divided into two groups: Group A: patients who underwent parent artery occlusion, and Group B: patients who underwent stent-assisted coil embolization. Follow-up outcomes were evaluated using the modified Rankin Scale (mRS). Results: After 12 months of follow-up, the favorable outcome (mRS: 0–2) had no statistical significance in both groups (p = 1.00). Patients in group A had greater ischemia compared with patients in group B, but the difference did not reach statistical significance (p = 0.421). In group B, patients had a higher rate of partial occlusion (p = 0.255) and recurrence (10% vs. 0%; p = 0.586). Conclusions: Stent-assisted coiling may not be superior to parent artery occlusion in selected patients after short-term follow-up. Parent artery occlusion is a simple, safe and effective treatment for large/giant internal carotid aneurysms. KEYWORDS: giant aneurysm, internal carotid aneurysm, parent artery occlusion, stent-assisted coiling
Introduction Giant/large internal carotid aneurysms are defined as the aneurysms greater than 25 mm and 15 mm, respectively. Giant/large intracranial aneurysms are not common and account for only 5% of all cerebral aneurysms [1]. The prognosis of untreatable giant/large intracranial aneurysms is poor and is associated with a 2-year mortality of 68% and 5-year mortality of 80% [2]. The pathogenesis remains unknown, therefore the treatment modalities are under debate. In the past, parent vessel occlusion with balloon or coils was performed in most cases and many reports confirm the favorable efficacy of this technique [3–5]. Recently, the emerging treatment of parent artery reconstruction (stent-assisted coiling, flow-diverting stent) has been used to resolve the special entity. Our present study aimed to review our expe-
Received 18 July 2014; revised 18 October 2014; accepted 23 November 2014. Correspondence: Dr Chuan-Zhi Duan, Department of Neurosurgery, Neurosurgery Institute, Key Laboratory on Brain Function Repair and Regeneration of Guangdong, Zhujiang Hospital, Southern Medical University, Guangzhou, China. E-mail: [email protected]
rience and gain insight into the advantages and risks of parent vessel occlusion and stent-assisted coiling for the treatment of giant/large internal carotid aneurysm.
Materials and methods We conducted a retrospective review of 39 consecutive patients with giant/large aneurysm of the internal carotid artery (ICA) who underwent endovascular treatment from 2006 to 2012. Patients with cerebral arteriovenous malformation were not included in our study. The type of therapy was not randomized, nor did it follow a specified protocol, and was decided by the discretion of neurosurgeon. All the patients were classified into two groups according to the treatment, Group A: 17 patients treated with parent vessel occlusion; and Group B: 22 patients with stent-assisted coil embolization. The clinical status of patients was assessed by the Hunt–Hess scale. For size assessment, the maximum diameter was measured on computed tomography, angiography or magnetic resonance angiography, including the thrombosed component if present. For dissecting aneurysms, size was evaluated as the maximum length 1
2
H. Li et al.
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Table 1. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17
Clinical condition and outcomes of patients with parent artery occlusion.
47/M 59/F 47/M 15/F 35/F 51/M 66/F 69/M 63/F 67/F 36/M 60/F 36/M 60/F 50/F 47/M 43/M
0 0 II 0 0 0 0 0 0 0 0 0 II II II II 0
25 15 16 40 23 20 32 20 31 45 48 21 21 19 18 20 18
L Cavernous R PCoA L PCoA L Cavernous L Cavernous L Supraclinoid R Cavernous R Cavernous R Cavernous L Cavernous L Cavernous L Supraclinoid L PCoA R PCoA R Cavernous R PCoA L cavernous
Unrupture Unrupture Rupture Unrupture Unrupture Unrupture Unrupture Unrupture Unrupture Unrupture Unrupture Unrupture Rupture Rupture Rupture Rupture Unrupture
Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Dissecting
13 10 19 9 6 12 12 9 7 9 12 9 29 21 5 11 9
10 12 9 12 12 6 12 10 9 9 12 15 6 9 15 13 10
Complete Complete Complete Complete Partial Complete Complete Complete Complete Complete Complete Complete Complete Complete Complete Complete Complete
None None None None None None None None None Aphasia None Numbness None None None None Aphasia
0 0 0 1 0 0 0 0 0 1 0 1 3 0 0 0 1
mRS Age/sex Hunt–Hess size (mm) Location Status Morphology Hospital stay (d) Follow-up (m) Occlusion Complication.
of the involved vessel. Patient demographics, aneurysm characteristics, treatment modalities, procedure-related complications and length of stay were recorded. During follow-up, patient outcome was also analyzed.
Preoperative evaluation Preoperatively, all patients underwent four-vessel angiography to confirm collateral circulation from the posterior and anterior communicating arteries. Balloon occlusion testing (BOT) was conventionally performed with non-detachable balloons (Balt 1, Balt Extrusion, Montmorency, France) in patients who underwent parent vessel occlusion. During the 30-min period of temporary ICA, both clinical evaluation and angiography were needed to test the tolerance of patient vessel occlusion. The clinical evaluation comprised patient’s sensation, motor activity and language ability, and angiographic evaluation was based on the delay of the venous phase of the examined and occluded vessels. Synchronous filling was a predictor for tolerance for permanent occlusion.
Follow-up The mean delay in follow-up was 10.7 ± 4.9 months (range: 6–36 months). The rate of occlusion was graded as complete if there was no opacification of the sac or neck of the aneurysm, and as partial if there was minor opacification in the neck. Clinical outcome was evaluated using the modified Rankin Scale (mRS) score through neurological examination or structured telephone interview. The clinical status of each patient at the last clinical follow-up was defined as the final outcome. We dichotomized outcomes as favorable (mRS: 0–2) and unfavorable (mRS: 3–5).
Statistical methods Analysis of continuous variables was performed by twotailed independent t-test or Wilcoxon’s two-sample test. Categorical variables were using Pear’s χ 2 test as appropriate. The level of statistical significance was p < 0.05. Statistical analysis was performed using SPSS for Windows (SPSS, Chicago, IL, USA).
Results Patient and aneurysm characteristics There were 24 women and 15 men, with an age range of 12–78 years (mean age was 52 years). The location of aneurysm was carotid cavernous in 14 patients, carotid supraclinoid segment in 14, posterior communicating artery in seven, and ophthalmic segment in four. Thirtyone aneurysms were large and eight were giant, and the mean size was 21.6 ± 7.4 mm (range 15–48 mm). The initial presentation was mass effect in 30 of 39 patients. Five patients presented with oculomotor nerve paresis, 11 with decreased visual acuity, six with limb numbness, and nine with subarachnoid hemorrhage (SAH). Nineteen patients complained of headache. The demographic and characteristics of aneurysm are summarized in Tables 1 and 2.
Angiographic follow-up In group A, permanent occlusion of the ICA was performed in 17 patients with good tolerance of BOT. Sixteen aneurysms were completely occluded, and one was partially obliterated with Guglielmi detachable coils (GDC). Detachable balloon occlusion was performed in nine patients and GDC in eight. During follow-up, there was no recurrence in group A. In group B, 16 International Journal of Neuroscience
How to treat giant/large internal carotid aneurysms
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Table 2. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22
3
Clinical condition and outcomes of patients with stent-assisted coiling. 58/M 52/F 46/M 52/F 57/F 64/F 34/M 57/M 46/F 52/F 72/F 65/F 64/F 31/M 54/F 75/F 60/F 78/F 48/F 41/F 60/M 12/M
0 0 0 0 0 0 0 0 II 0 0 0 0 0 II 0 0 II 0 0 0 II
18 20 21 20 25 15 20 18 15 19 15 17 15 35 15 25 19 17 22 20 21 19
L Ophthalmic L Ophthalmic R Ophthalmic L Supraclinoid R Cavernous L Cavernous R Supraclinoid L Supraclinoid R Supraclinoid L Supraclinoid L Supraclinoid L Supraclinoid L Supraclinoid L Supraclinoid R PCoA R PCoA R Supraclinoid R Supraclinoid L Supraclinoid L Ophthalmic R Cavernous R Cavernous
Unrupture Unrupture Unrupture Unrupture Unrupture Unrupture Unrupture Unrupture Rupture Unrupture Unrupture Unrupture Unrupture Unrupture Rupture Unrupture Unrupture Rupture Unrupture Unrupture Unrupture Rupture
Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Dissecting Dissecting Saccular Saccular Saccular Saccular Saccular Dissecting Dissecting
6 11 14 8 7 10 13 8 6 7 8 7 17 8 6 7 3 27 4 7 10 34
6 12 12 9 15 9 36 12 12 12 6 6 12 6 9 10 9 12 6 6 12 9
Complete Complete Partial Complete Complete Complete Partial Complete Partial Complete Complete Partial Complete Complete Complete Complete Complete Complete Complete Complete Complete Complete
None Regrowth None None None None None None None None Aphasia None None None None None None None None None None None
0 1 0 0 0 0 0 1 3 0 1 1 0 0 0 0 0 3 0 0 0 0
mRS Age/sex Hunt–Hess Size (mm) Location Status Morphology Hospital stay (d) Follow-up (m) Occlusion Complication
patients had complete occlusion and six had partial occlusion. During follow-up, 18 of the 22 patients had complete occlusion, two aneurysms developed recurrence at 12 months, there was marked filling of the aneurismal sac, and additional coils were placed again to occlude aneurysm (Figure 1).
Clinical follow-up Clinical outcome was favorable in 36 of the 39 patients. In group A, one patient developed transient aphasia, although the symptom disappeared before discharge. One patient developed right limb numbness after the procedure, but during follow-up the symptom was greatly improved (Figure 2). In group B, one patient had transient numbness of right limb after the procedure, but the symptom disappeared before discharge.
Comparability of study groups There were no significant differences in age, gender distribution, morphology, the Hunt–Hess score, or size and rupture status of aneurysms between the groups (Table 3). After 12 months of follow-up, the favorable outcome (mRvvS: 0–2) had no statistically significant difference in both groups (p = 1.00). Patients in group A had greater ischemia compared with patients in group B, but the difference was not significant (p = 0.421). In Group B, patients had a higher rate of partial occlusion (p = 0.255) and recurrence (p = 0.586). Patient outcomes are shown in Table 4. C
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Discussion Giant/large aneurysms are a special subgroup of intracranial aneurysms whose maximum diameters are greater than 25 mm and 15 mm, respectively. These are usually present in men; however, ICA aneurysms have a female preponderance [6]. It is reported that two-thirds of giant aneurysms arise in the anterior circulation and one-third in the posterior circulation. In the ICA, the carotid siphon is the most frequent location of aneurysm [7]. As a result of the unfavorable prognosis of untreatable giant aneurysm of the ICA, surgical or endovascular treatment is warranted to reduce the risk of rupture. However, due to their giant size, partial thrombosis and wide neck, the optimal therapy is under debate. Treatment mainly includes deconstructive therapy (parent artery occlusion) and reconstructive therapy (stentassisted coiling, flow diverting stent). Compared with selective coiling, parent artery occlusion can significantly decrease the intra- aneurysmal pressure, leading to stasis and immediate thrombosis. In addition, it can also improve the symptoms by alleviating the mass effect owing to the reduction of pulsation and shrinkage of anuerysmal sac. Parent artery occlusion is referred as one of the most reliable techniques to prevent rebleeding. Clarencon et al. [8] reported treatment of 26 ICA aneurysms with parent artery occlusion, and clinical symptoms disappeared in 19 patients, and no patients developed worsening of symptoms. De Gast et al. reported alleviation mass effect symptoms in 91% of patients, and there were no early or late complications of carotid artery occlusion [9]. In our series, 16
H. Li et al.
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A 52-year-old woman with ophthalmic aneurysm of the left ICA. (A) Anteroposterior angiography showed a large ophthalmic aneurysm of the left ICA. (B) The process of embolization with stent-assisted coiling. (C) The aneurysm was almost completely embolized with patency of the parent artery. (D) Anteroposterior angiography showed aneurysmal regrowth during 12 months follow-up. (E) Anteroposterior angiography showed that additional coils were placed to complete the occlusion of aneurysm.
Figure 1.
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How to treat giant/large internal carotid aneurysms
A 15-year-old woman with cavernous aneurysm of the left ICA. (A) Digital subtraction angiography (DSA) showed a 4.0 × 3.0 cm cavernous aneurysm (anteroposterior view). (B) After compression of the left common carotid artery, anteroposterior angiography showed that the right ICA supplied the left anterior cerebral artery and middle cerebral artery territories through the anterior communicating artery. (C) DSA showed that the left ICA was successfully occluded with two balloons. (D) The left anterior cerebral artery and middle cerebral artery territories were well compensated during 12 months follow-up. (E) Magnetic resonance spectroscopy showed that the left blood supply territory was slightly decreased compared with the right one. (F) MRI showed that there was no significant cerebral infarct in the left hemisphere.
Figure 2.
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Table 3. groups.
Population and aneurysm characteristics of both
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Variable Sex Male Female Age (years) Diameter (mm) Hunt–Hess Milda Moderateb Severec Rupture state Rupture Unrupture Type Saccular Dissecting
Group A (n = 17)
Group B (n = 22)
8 (47.1%) 9 (52.9%) 50.0 ± 3.5 24.6 ± 10.3
7 (31.8%) 15 (68.2%) 53.7 ± 3.2 20.3 ± 4.4
12 (70.6%) 3 (17.6%) 2 (11.8%)
18 (76.9%) 3 (15.4%) 1 (7.7%)
5 (29.4%) 12 (70.6%)
4 (18.2%) 18 (81.8%)
16 (94.1%) 1 (5.9%)
18 (81.8%) 4 (18.2%)
p 0.332
0.447 0.084 0.635
0.658
a
Mild: Hunt–Hess 0, Hunt–Hess III–V.
b
moderate: Hunt–Hess I–II
0.512 c
severe:
patients had favorable outcome without any neurological deficits after the procedure, which concurred with the previous report [5]. We concluded that ICA occlusion in the acute phase of SAH is not advisable because vasospasm secondary to SAH can be aggravated by diminished reserve capacity, which further enhances the risk of ischemia. We suggest that initial partial coiling of aneurysm at acute phase and parent artery occlusion in the late phase may improve patient outcome. Although parent artery occlusion is an effective method for treating giant ICA aneurysms, there are some complications with the procedure. Cerebral infarction is the most frequent complication of ICA occlusion. Van der Schaaf et al. [10] reported that the incidence of early complications leading to permanent Table 4. Univariate statistical models comparing the outcomes of both groups. Variable
Group A (n = 17) Group B (n = 22)
Hospital stay (d) Outcomes Favorable Unfavorable Ischemia Yes No Occlusion Complete Partial Recurrence Yes No
11.9 ± 6.0
10.3 ± 7.3
16 (94.1%) 1 (5.8%)
20 (90.0%) 2 (10.0%)
3 (17.6%) 14 (82.4%)
1 (4.5%) 21 (95.5%)
16 (94.1%) 1 (5.9%)
18 (81.8%) 4 (18.2%)
0 (0%) 17 (100%)
2 (10%) 20 (90%)
a b
p 0.105a 1.00b 0.421b 0.255b 0.586b
Mann–Whitney U test. Pearson’s χ 2 test.
neurological deficit was 1.6%, while late morbidity was 3.4%. Blanc et al. [11] reported that one patient developed delayed stroke secondary to increasing mass effect after the procedure, which may be explained by the release of inflammatory mediators such as vascular endothelial growth factor. In our series, one patient developed transient aphasia and another developed left limb numbness after the procedure. Magnetic resonance spectroscopy showed that the left blood supply territory was slightly decreased, but Magnetic resonance imaging (MRI) showed that there was no significant cerebral infarct in the left hemisphere, thus we concluded that angiographic compensation might not completely estimate ischemia. It is acknowledged that the basic therapeutic aim in aneurysm is complete occlusion with the preservation of parent artery and branches. Recently, with the development of new endovascular techniques, occlusion of aneurysm while preserving the patency of ICA has become available, especially in wide neck, large or dissecting aneurysms. However, reports about treating giant ICA aneurysms with stent-assisted coiling are not common. Ha and Jang reported three patients with giant ICA aneurysms who were treated by stent-assisted coiling, and all of them showed good clinical outcome [12]. Hauck et al. reported five of the 11 patients with large or giant ophthalmic and cavernous aneurysm had partial occlusion after the procedure [13]. In our series, one patient developed transient numbness of the right limb. It may be that stent placement decreased the incidence of ischemic events after systemic anticoagulation therapy, but because of the limited number of cases, we found no significant difference (p = 0.421). It is reported that compared with small aneurysms, there is higher recanalization duo to neck residual in giant/large aneurysms, especially if they are partially thrombosed. It is acknowledged that packing density is the key element in decreasing the recurrence rate. Hauck et al. reported that six of the 11 patients with giant intracranial aneurysms had complete or near-complete occlusion on postoperative angiography during follow-up [13]. Morita reported three patients with giant ICA aneurysm were treated with stentassisted coiling but none of them had favorable clinical outcome, and two needed treatment for ICA occlusion [14]. In our study, the occlusion rate did not reach statistical significance in either group; patients in group B had more partial occlusion (18.2% vs. 5.9%) and recurrence (10% vs. 0%), two ophthalmic segment aneurysms developed recurrence during 12 months follow-up, and additional coils were placed again to obliterate the aneurysm. As a result of the limited number of cases, we found no correlation between partial occlusion and recurrence, therefore we recommend that aneurysms with partial occlusion should be International Journal of Neuroscience
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How to treat giant/large internal carotid aneurysms
checked regularly. In partially thrombosed aneurysms, coils tended to migrate into soft intra-aneurysmal thrombosis, which may be relevant for recanalization. In our experience, because of the large size of aneurysm, current stenting may be insufficient to divert inflow into the aneurysm, which increases the risk of recanalization, and new low-porosity stenting is a promising option. Fortunately, in recent years, new devices, such as flow-diverting stents, have provided new insight into treating giant ICA aneurysms. Szikora et al. reported 18 patients with wide-necked large or giant aneurysms who were treated with a pipeline embolization device (PED), and the complete occlusion rate was 94.4% at 6 months follow-up [15]. Becske et al. reported 108 patients with uncoilable aneurysms that were treated by PED, and only six patients experienced neurological events. They concluded that PED is an effective treatment of giant ICA aneurysm [16]. However, stent migration and aneurysmal rupture also occurred in patients with giant ICA aneurysms [17,18]. So far, longterm follow-up in patients with giant aneurysms treated by flow-diverting stent is lacking, and the efficacy of this technique needs to be evaluated in more cases. There were some limitations to our study. First, because of the retrospective nature of analysis, inherent bias may not be avoided, which excluded randomization. Second, the limited dates may not be large enough to draw definitive conclusions.
Conclusions The short-term follow-up results demonstrated that stent-assisted coiling showed no superiority compared with parent artery occlusion in selected patients. Parent artery occlusion was a simple, safe and effective treatment for large/giant ICA aneurysms, and we expect long-term follow-up results to verify the efficiency of both modalities.
Declaration of Interest The authors declare that they have no conflict of interest. The authors alone are responsible for the content and writing of this paper.
References 1. Lubicz B, Gauvrit JY, Leclerc X, et al. Giant aneurysms of the internal carotid artery: endovascular treatment and long-term follow-up. Neuroradiology 2003;45:650–55.
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2. Drake CG. Giant intracranial aneurysms: experience with surgical treatment in 174 patients. Clin Neurosurg 1979;26: 12–95. 3. Higashida RT, Halbach VV, Dowd C, et al. Endovascular detachable balloon embolization therapy of cavernous carotid artery aneurysms: results in 87 cases. J Neurosurg 1990;72:857–63. 4. Graves VB, Perl JN, Strother CM, et al. Endovascular occlusion of the carotid or vertebral artery with temporary proximal flow arrest and microcoils: clinical results. Am J Neuroradiol (AJNR) 1997;18:1201–206. 5. Higashida RT, Halbach VV, Dowd CF, et al. Intracranial aneurysms: interventional neurovascular treatment with detachable balloons–results in 215 cases. Radiology 1991;178: 663–70. 6. Lv X, Jiang C, Li Y, et al. Treatment of giant intracranial aneurysms. Intervent Neuroradiol 2009;15:135–44. 7. Choi IS, David C. Giant intracranial aneurysms: development, clinical presentation and treatment. Eur J Radiol 2003;46:178–94. 8. Clarencon F, Bonneville F, Boch AL, et al. Parent artery occlusion is not obsolete in giant aneurysms of the ICA. Experience with very-long-term follow-up. Neuroradiology 2011;53:973–82. 9. de Gast AN, Sprengers ME, van Rooij WJ, et al. Midterm clinical and magnetic resonance imaging follow-up of large and giant carotid artery aneurysms after therapeutic carotid artery occlusion. Neurosurgery 2007;60:1025–31. 10. van der Schaaf IC, Brilstra EH, Buskens E, et al. Endovascular treatment of aneurysms in the cavernous sinus: a systematic review on balloon occlusion of the parent vessel and embolization with coils. Stroke 2002;33:313–18. 11. Blanc R, Weill A, Piotin M, et al. Delayed stroke secondary to increasing mass effect after endovascular treatment of a giant aneurysm by parent vessel occlusion. Am J Neuroradiol (AJNR) 2001;22:1841–43. 12. Ha SW, Jang SJ. Clinical analysis of giant intracranial aneurysms with endovascular embolization. J Cerebrovasc Endovasc Neurosurg 2012;14:22–8. 13. Hauck EF, Welch BG, White JA, et al. Stent/coil treatment of very large and giant unruptured ophthalmic and cavernous aneurysms. Surg Neurol 2009;71:19–24. 14. Morita K, Sorimachi T, Ito Y, et al. Intra-aneurysmal coil embolization for large or giant carotid artery aneurysms in the cavernous sinus. Neurol Med Chir (Tokyo) 2011;51: 762–66. 15. Szikora I, Berentei Z, Kulcsar Z, et al. Treatment of intracranial aneurysms by functional reconstruction of the parent artery: the Budapest experience with the pipeline embolization device. Am J Neuroradiol (AJNR) 2010;31: 1139–47. 16. Becske T, Kallmes DF, Saatci I, et al. Pipeline for uncoilable or failed aneurysms: results from a multicenter clinical trial. Radiology 2013;267:858–68. 17. Chalouhi N, Satti SR, Tjoumakaris S, et al. Delayed migration of a pipeline embolization device. Neurosurgery 2013;72:s229–34. 18. Kan P, Siddiqui AH, Veznedaroglu E, et al. Early postmarket results after treatment of intracranial aneurysms with the pipeline embolization device: a US multicenter experience. Neurosurgery 2012;71:1080–88.
ORIGINAL ARTICLE
Treatment of giant/large internal carotid aneurysms: parent artery occlusion or stent-assisted coiling
Int J Neurosci Downloaded from informahealthcare.com by University of Massachusetts on 03/13/15 For personal use only.
Hui Li, Xu-Ying He, Xi-Feng Li, Xin Zhang, Yan-Chao Liu, and Chuan-Zhi Duan Department of Neurosurgery, Neurosurgery Institute, Key Laboratory on Brain Function, Repair and Regeneration of Guangdong, Zhujiang Hospital, Southern Medical University, Guangzhou, China Purpose: Treatment of giant/large internal carotid aneurysm is a challenge for neurologists. Previously, parent artery occlusion was the classic therapy; now the stent-assisted coil embolization has become available in recent years, but the optimal therapy is under debate. The goal of the present study was to compare two endovascular treatment modalities in terms of safety, efficacy and short-term outcomes. Methods: All the patients were divided into two groups: Group A: patients who underwent parent artery occlusion, and Group B: patients who underwent stent-assisted coil embolization. Follow-up outcomes were evaluated using the modified Rankin Scale (mRS). Results: After 12 months of follow-up, the favorable outcome (mRS: 0–2) had no statistical significance in both groups (p = 1.00). Patients in group A had greater ischemia compared with patients in group B, but the difference did not reach statistical significance (p = 0.421). In group B, patients had a higher rate of partial occlusion (p = 0.255) and recurrence (10% vs. 0%; p = 0.586). Conclusions: Stent-assisted coiling may not be superior to parent artery occlusion in selected patients after short-term follow-up. Parent artery occlusion is a simple, safe and effective treatment for large/giant internal carotid aneurysms. KEYWORDS: giant aneurysm, internal carotid aneurysm, parent artery occlusion, stent-assisted coiling
Introduction Giant/large internal carotid aneurysms are defined as the aneurysms greater than 25 mm and 15 mm, respectively. Giant/large intracranial aneurysms are not common and account for only 5% of all cerebral aneurysms [1]. The prognosis of untreatable giant/large intracranial aneurysms is poor and is associated with a 2-year mortality of 68% and 5-year mortality of 80% [2]. The pathogenesis remains unknown, therefore the treatment modalities are under debate. In the past, parent vessel occlusion with balloon or coils was performed in most cases and many reports confirm the favorable efficacy of this technique [3–5]. Recently, the emerging treatment of parent artery reconstruction (stent-assisted coiling, flow-diverting stent) has been used to resolve the special entity. Our present study aimed to review our expe-
Received 18 July 2014; revised 18 October 2014; accepted 23 November 2014. Correspondence: Dr Chuan-Zhi Duan, Department of Neurosurgery, Neurosurgery Institute, Key Laboratory on Brain Function Repair and Regeneration of Guangdong, Zhujiang Hospital, Southern Medical University, Guangzhou, China. E-mail: [email protected]
rience and gain insight into the advantages and risks of parent vessel occlusion and stent-assisted coiling for the treatment of giant/large internal carotid aneurysm.
Materials and methods We conducted a retrospective review of 39 consecutive patients with giant/large aneurysm of the internal carotid artery (ICA) who underwent endovascular treatment from 2006 to 2012. Patients with cerebral arteriovenous malformation were not included in our study. The type of therapy was not randomized, nor did it follow a specified protocol, and was decided by the discretion of neurosurgeon. All the patients were classified into two groups according to the treatment, Group A: 17 patients treated with parent vessel occlusion; and Group B: 22 patients with stent-assisted coil embolization. The clinical status of patients was assessed by the Hunt–Hess scale. For size assessment, the maximum diameter was measured on computed tomography, angiography or magnetic resonance angiography, including the thrombosed component if present. For dissecting aneurysms, size was evaluated as the maximum length 1
2
H. Li et al.
Int J Neurosci Downloaded from informahealthcare.com by University of Massachusetts on 03/13/15 For personal use only.
Table 1. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17
Clinical condition and outcomes of patients with parent artery occlusion.
47/M 59/F 47/M 15/F 35/F 51/M 66/F 69/M 63/F 67/F 36/M 60/F 36/M 60/F 50/F 47/M 43/M
0 0 II 0 0 0 0 0 0 0 0 0 II II II II 0
25 15 16 40 23 20 32 20 31 45 48 21 21 19 18 20 18
L Cavernous R PCoA L PCoA L Cavernous L Cavernous L Supraclinoid R Cavernous R Cavernous R Cavernous L Cavernous L Cavernous L Supraclinoid L PCoA R PCoA R Cavernous R PCoA L cavernous
Unrupture Unrupture Rupture Unrupture Unrupture Unrupture Unrupture Unrupture Unrupture Unrupture Unrupture Unrupture Rupture Rupture Rupture Rupture Unrupture
Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Dissecting
13 10 19 9 6 12 12 9 7 9 12 9 29 21 5 11 9
10 12 9 12 12 6 12 10 9 9 12 15 6 9 15 13 10
Complete Complete Complete Complete Partial Complete Complete Complete Complete Complete Complete Complete Complete Complete Complete Complete Complete
None None None None None None None None None Aphasia None Numbness None None None None Aphasia
0 0 0 1 0 0 0 0 0 1 0 1 3 0 0 0 1
mRS Age/sex Hunt–Hess size (mm) Location Status Morphology Hospital stay (d) Follow-up (m) Occlusion Complication.
of the involved vessel. Patient demographics, aneurysm characteristics, treatment modalities, procedure-related complications and length of stay were recorded. During follow-up, patient outcome was also analyzed.
Preoperative evaluation Preoperatively, all patients underwent four-vessel angiography to confirm collateral circulation from the posterior and anterior communicating arteries. Balloon occlusion testing (BOT) was conventionally performed with non-detachable balloons (Balt 1, Balt Extrusion, Montmorency, France) in patients who underwent parent vessel occlusion. During the 30-min period of temporary ICA, both clinical evaluation and angiography were needed to test the tolerance of patient vessel occlusion. The clinical evaluation comprised patient’s sensation, motor activity and language ability, and angiographic evaluation was based on the delay of the venous phase of the examined and occluded vessels. Synchronous filling was a predictor for tolerance for permanent occlusion.
Follow-up The mean delay in follow-up was 10.7 ± 4.9 months (range: 6–36 months). The rate of occlusion was graded as complete if there was no opacification of the sac or neck of the aneurysm, and as partial if there was minor opacification in the neck. Clinical outcome was evaluated using the modified Rankin Scale (mRS) score through neurological examination or structured telephone interview. The clinical status of each patient at the last clinical follow-up was defined as the final outcome. We dichotomized outcomes as favorable (mRS: 0–2) and unfavorable (mRS: 3–5).
Statistical methods Analysis of continuous variables was performed by twotailed independent t-test or Wilcoxon’s two-sample test. Categorical variables were using Pear’s χ 2 test as appropriate. The level of statistical significance was p < 0.05. Statistical analysis was performed using SPSS for Windows (SPSS, Chicago, IL, USA).
Results Patient and aneurysm characteristics There were 24 women and 15 men, with an age range of 12–78 years (mean age was 52 years). The location of aneurysm was carotid cavernous in 14 patients, carotid supraclinoid segment in 14, posterior communicating artery in seven, and ophthalmic segment in four. Thirtyone aneurysms were large and eight were giant, and the mean size was 21.6 ± 7.4 mm (range 15–48 mm). The initial presentation was mass effect in 30 of 39 patients. Five patients presented with oculomotor nerve paresis, 11 with decreased visual acuity, six with limb numbness, and nine with subarachnoid hemorrhage (SAH). Nineteen patients complained of headache. The demographic and characteristics of aneurysm are summarized in Tables 1 and 2.
Angiographic follow-up In group A, permanent occlusion of the ICA was performed in 17 patients with good tolerance of BOT. Sixteen aneurysms were completely occluded, and one was partially obliterated with Guglielmi detachable coils (GDC). Detachable balloon occlusion was performed in nine patients and GDC in eight. During follow-up, there was no recurrence in group A. In group B, 16 International Journal of Neuroscience
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Table 2. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22
3
Clinical condition and outcomes of patients with stent-assisted coiling. 58/M 52/F 46/M 52/F 57/F 64/F 34/M 57/M 46/F 52/F 72/F 65/F 64/F 31/M 54/F 75/F 60/F 78/F 48/F 41/F 60/M 12/M
0 0 0 0 0 0 0 0 II 0 0 0 0 0 II 0 0 II 0 0 0 II
18 20 21 20 25 15 20 18 15 19 15 17 15 35 15 25 19 17 22 20 21 19
L Ophthalmic L Ophthalmic R Ophthalmic L Supraclinoid R Cavernous L Cavernous R Supraclinoid L Supraclinoid R Supraclinoid L Supraclinoid L Supraclinoid L Supraclinoid L Supraclinoid L Supraclinoid R PCoA R PCoA R Supraclinoid R Supraclinoid L Supraclinoid L Ophthalmic R Cavernous R Cavernous
Unrupture Unrupture Unrupture Unrupture Unrupture Unrupture Unrupture Unrupture Rupture Unrupture Unrupture Unrupture Unrupture Unrupture Rupture Unrupture Unrupture Rupture Unrupture Unrupture Unrupture Rupture
Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Saccular Dissecting Dissecting Saccular Saccular Saccular Saccular Saccular Dissecting Dissecting
6 11 14 8 7 10 13 8 6 7 8 7 17 8 6 7 3 27 4 7 10 34
6 12 12 9 15 9 36 12 12 12 6 6 12 6 9 10 9 12 6 6 12 9
Complete Complete Partial Complete Complete Complete Partial Complete Partial Complete Complete Partial Complete Complete Complete Complete Complete Complete Complete Complete Complete Complete
None Regrowth None None None None None None None None Aphasia None None None None None None None None None None None
0 1 0 0 0 0 0 1 3 0 1 1 0 0 0 0 0 3 0 0 0 0
mRS Age/sex Hunt–Hess Size (mm) Location Status Morphology Hospital stay (d) Follow-up (m) Occlusion Complication
patients had complete occlusion and six had partial occlusion. During follow-up, 18 of the 22 patients had complete occlusion, two aneurysms developed recurrence at 12 months, there was marked filling of the aneurismal sac, and additional coils were placed again to occlude aneurysm (Figure 1).
Clinical follow-up Clinical outcome was favorable in 36 of the 39 patients. In group A, one patient developed transient aphasia, although the symptom disappeared before discharge. One patient developed right limb numbness after the procedure, but during follow-up the symptom was greatly improved (Figure 2). In group B, one patient had transient numbness of right limb after the procedure, but the symptom disappeared before discharge.
Comparability of study groups There were no significant differences in age, gender distribution, morphology, the Hunt–Hess score, or size and rupture status of aneurysms between the groups (Table 3). After 12 months of follow-up, the favorable outcome (mRvvS: 0–2) had no statistically significant difference in both groups (p = 1.00). Patients in group A had greater ischemia compared with patients in group B, but the difference was not significant (p = 0.421). In Group B, patients had a higher rate of partial occlusion (p = 0.255) and recurrence (p = 0.586). Patient outcomes are shown in Table 4. C
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Discussion Giant/large aneurysms are a special subgroup of intracranial aneurysms whose maximum diameters are greater than 25 mm and 15 mm, respectively. These are usually present in men; however, ICA aneurysms have a female preponderance [6]. It is reported that two-thirds of giant aneurysms arise in the anterior circulation and one-third in the posterior circulation. In the ICA, the carotid siphon is the most frequent location of aneurysm [7]. As a result of the unfavorable prognosis of untreatable giant aneurysm of the ICA, surgical or endovascular treatment is warranted to reduce the risk of rupture. However, due to their giant size, partial thrombosis and wide neck, the optimal therapy is under debate. Treatment mainly includes deconstructive therapy (parent artery occlusion) and reconstructive therapy (stentassisted coiling, flow diverting stent). Compared with selective coiling, parent artery occlusion can significantly decrease the intra- aneurysmal pressure, leading to stasis and immediate thrombosis. In addition, it can also improve the symptoms by alleviating the mass effect owing to the reduction of pulsation and shrinkage of anuerysmal sac. Parent artery occlusion is referred as one of the most reliable techniques to prevent rebleeding. Clarencon et al. [8] reported treatment of 26 ICA aneurysms with parent artery occlusion, and clinical symptoms disappeared in 19 patients, and no patients developed worsening of symptoms. De Gast et al. reported alleviation mass effect symptoms in 91% of patients, and there were no early or late complications of carotid artery occlusion [9]. In our series, 16
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A 52-year-old woman with ophthalmic aneurysm of the left ICA. (A) Anteroposterior angiography showed a large ophthalmic aneurysm of the left ICA. (B) The process of embolization with stent-assisted coiling. (C) The aneurysm was almost completely embolized with patency of the parent artery. (D) Anteroposterior angiography showed aneurysmal regrowth during 12 months follow-up. (E) Anteroposterior angiography showed that additional coils were placed to complete the occlusion of aneurysm.
Figure 1.
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How to treat giant/large internal carotid aneurysms
A 15-year-old woman with cavernous aneurysm of the left ICA. (A) Digital subtraction angiography (DSA) showed a 4.0 × 3.0 cm cavernous aneurysm (anteroposterior view). (B) After compression of the left common carotid artery, anteroposterior angiography showed that the right ICA supplied the left anterior cerebral artery and middle cerebral artery territories through the anterior communicating artery. (C) DSA showed that the left ICA was successfully occluded with two balloons. (D) The left anterior cerebral artery and middle cerebral artery territories were well compensated during 12 months follow-up. (E) Magnetic resonance spectroscopy showed that the left blood supply territory was slightly decreased compared with the right one. (F) MRI showed that there was no significant cerebral infarct in the left hemisphere.
Figure 2.
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Table 3. groups.
Population and aneurysm characteristics of both
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Variable Sex Male Female Age (years) Diameter (mm) Hunt–Hess Milda Moderateb Severec Rupture state Rupture Unrupture Type Saccular Dissecting
Group A (n = 17)
Group B (n = 22)
8 (47.1%) 9 (52.9%) 50.0 ± 3.5 24.6 ± 10.3
7 (31.8%) 15 (68.2%) 53.7 ± 3.2 20.3 ± 4.4
12 (70.6%) 3 (17.6%) 2 (11.8%)
18 (76.9%) 3 (15.4%) 1 (7.7%)
5 (29.4%) 12 (70.6%)
4 (18.2%) 18 (81.8%)
16 (94.1%) 1 (5.9%)
18 (81.8%) 4 (18.2%)
p 0.332
0.447 0.084 0.635
0.658
a
Mild: Hunt–Hess 0, Hunt–Hess III–V.
b
moderate: Hunt–Hess I–II
0.512 c
severe:
patients had favorable outcome without any neurological deficits after the procedure, which concurred with the previous report [5]. We concluded that ICA occlusion in the acute phase of SAH is not advisable because vasospasm secondary to SAH can be aggravated by diminished reserve capacity, which further enhances the risk of ischemia. We suggest that initial partial coiling of aneurysm at acute phase and parent artery occlusion in the late phase may improve patient outcome. Although parent artery occlusion is an effective method for treating giant ICA aneurysms, there are some complications with the procedure. Cerebral infarction is the most frequent complication of ICA occlusion. Van der Schaaf et al. [10] reported that the incidence of early complications leading to permanent Table 4. Univariate statistical models comparing the outcomes of both groups. Variable
Group A (n = 17) Group B (n = 22)
Hospital stay (d) Outcomes Favorable Unfavorable Ischemia Yes No Occlusion Complete Partial Recurrence Yes No
11.9 ± 6.0
10.3 ± 7.3
16 (94.1%) 1 (5.8%)
20 (90.0%) 2 (10.0%)
3 (17.6%) 14 (82.4%)
1 (4.5%) 21 (95.5%)
16 (94.1%) 1 (5.9%)
18 (81.8%) 4 (18.2%)
0 (0%) 17 (100%)
2 (10%) 20 (90%)
a b
p 0.105a 1.00b 0.421b 0.255b 0.586b
Mann–Whitney U test. Pearson’s χ 2 test.
neurological deficit was 1.6%, while late morbidity was 3.4%. Blanc et al. [11] reported that one patient developed delayed stroke secondary to increasing mass effect after the procedure, which may be explained by the release of inflammatory mediators such as vascular endothelial growth factor. In our series, one patient developed transient aphasia and another developed left limb numbness after the procedure. Magnetic resonance spectroscopy showed that the left blood supply territory was slightly decreased, but Magnetic resonance imaging (MRI) showed that there was no significant cerebral infarct in the left hemisphere, thus we concluded that angiographic compensation might not completely estimate ischemia. It is acknowledged that the basic therapeutic aim in aneurysm is complete occlusion with the preservation of parent artery and branches. Recently, with the development of new endovascular techniques, occlusion of aneurysm while preserving the patency of ICA has become available, especially in wide neck, large or dissecting aneurysms. However, reports about treating giant ICA aneurysms with stent-assisted coiling are not common. Ha and Jang reported three patients with giant ICA aneurysms who were treated by stent-assisted coiling, and all of them showed good clinical outcome [12]. Hauck et al. reported five of the 11 patients with large or giant ophthalmic and cavernous aneurysm had partial occlusion after the procedure [13]. In our series, one patient developed transient numbness of the right limb. It may be that stent placement decreased the incidence of ischemic events after systemic anticoagulation therapy, but because of the limited number of cases, we found no significant difference (p = 0.421). It is reported that compared with small aneurysms, there is higher recanalization duo to neck residual in giant/large aneurysms, especially if they are partially thrombosed. It is acknowledged that packing density is the key element in decreasing the recurrence rate. Hauck et al. reported that six of the 11 patients with giant intracranial aneurysms had complete or near-complete occlusion on postoperative angiography during follow-up [13]. Morita reported three patients with giant ICA aneurysm were treated with stentassisted coiling but none of them had favorable clinical outcome, and two needed treatment for ICA occlusion [14]. In our study, the occlusion rate did not reach statistical significance in either group; patients in group B had more partial occlusion (18.2% vs. 5.9%) and recurrence (10% vs. 0%), two ophthalmic segment aneurysms developed recurrence during 12 months follow-up, and additional coils were placed again to obliterate the aneurysm. As a result of the limited number of cases, we found no correlation between partial occlusion and recurrence, therefore we recommend that aneurysms with partial occlusion should be International Journal of Neuroscience
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How to treat giant/large internal carotid aneurysms
checked regularly. In partially thrombosed aneurysms, coils tended to migrate into soft intra-aneurysmal thrombosis, which may be relevant for recanalization. In our experience, because of the large size of aneurysm, current stenting may be insufficient to divert inflow into the aneurysm, which increases the risk of recanalization, and new low-porosity stenting is a promising option. Fortunately, in recent years, new devices, such as flow-diverting stents, have provided new insight into treating giant ICA aneurysms. Szikora et al. reported 18 patients with wide-necked large or giant aneurysms who were treated with a pipeline embolization device (PED), and the complete occlusion rate was 94.4% at 6 months follow-up [15]. Becske et al. reported 108 patients with uncoilable aneurysms that were treated by PED, and only six patients experienced neurological events. They concluded that PED is an effective treatment of giant ICA aneurysm [16]. However, stent migration and aneurysmal rupture also occurred in patients with giant ICA aneurysms [17,18]. So far, longterm follow-up in patients with giant aneurysms treated by flow-diverting stent is lacking, and the efficacy of this technique needs to be evaluated in more cases. There were some limitations to our study. First, because of the retrospective nature of analysis, inherent bias may not be avoided, which excluded randomization. Second, the limited dates may not be large enough to draw definitive conclusions.
Conclusions The short-term follow-up results demonstrated that stent-assisted coiling showed no superiority compared with parent artery occlusion in selected patients. Parent artery occlusion was a simple, safe and effective treatment for large/giant ICA aneurysms, and we expect long-term follow-up results to verify the efficiency of both modalities.
Declaration of Interest The authors declare that they have no conflict of interest. The authors alone are responsible for the content and writing of this paper.
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