Endovascular treatment of ruptured vertebrobasilar dissecting aneurysms: Review of 40 consecutive cases
Correspondence Address: Source of Support: None, Conflict of Interest: None DOI: 10.4103/0028-3886.178043
Source of Support: None, Conflict of Interest: None
Aims: To evaluate the safety and efficacy of endovascular intervention in the treatment of ruptured vertebrobasilar dissecting aneurysms (VBDAs) with the aim of developing endovascular treatment standards for this disorder.
Keywords: Aneurysms; dissection; stent; subarachnoid hemorrhage; technique
Vertebrobasilar dissecting aneurysms (VBDAs) are uncommon lesions that may lead to a life-threatening subarachnoid hemorrhage (SAH). , Ruptured VBDAs require an early surgical intervention given the substantial risk of rebleeding after the first hemorrhage. ,, Such interventions include both surgical as well as endovascular exclusion of the lesion. Although surgical intervention is still being practiced, its use is steadily declining for posterior circulation dissecting aneurysms owing to the relatively high complication rate associated with surgical intervention.  In contrast, the endovascular treatment, including parent artery occlusion (proximal arterial occlusion and internal trapping), and stent implantation (with or without additional coiling), has emerged as a major therapeutic option. ,,,, Internal trapping is generally considered as the most reliable treatment, but is not suitable for all patients.  A stent alone therapy is controversial mainly because of its relatively high rebleeding rate.  The safety and efficacy of stent-assisted coiling also remain unproven.  The endovascular therapeutic strategies for ruptured VBDAs remain controversial, and few studies are available reporting on both the moderate-term or long-term results of endovascular treatment for ruptured VBDAs. The general treatment guidelines for ruptured VBDAs have not been devised, and no randomized trial data exist. In this retrospective study, we present the initial angiographic features, the modalities of endovascular treatment, and the clinical outcomes in 40 consecutive patients with ruptured VBDAs, and propose a novel morphological classification of VBDAs to guide the coil and stent placement. This classification is proposed with the objective of establishing endovascular treatment standards for ruptured VBDAs.
All medical data were acquired for diagnostic purposes, and the Ethics Committee of our hospital approved of this retrospective study.
Patients and data collection
We reviewed the patient database in our hospital from January 2010 to June 2014 and identified 40 consecutive patients diagnosed with a VBDA, who developed a SAH and in whom an endovascular interventional procedure was undertaken. All patients included in this study met the following inclusion criteria: (1) A history of SAH or the occurrence of an intracerebral hematoma related to the presence of an intracranial VBDA, which was confirmed by the digital subtraction angiography (DSA) or magnetic resonance imaging (MRI); (2) This aneurysm was treated by an endovascular approach. The exclusion criteria included: (1) A history of trauma or iatrogenic injury; (2) the presence of fibromuscular dysplasia; (3) the patients with no clinical follow-up. The information collected and analyzed included patient demographics (age and sex), Hunt and Hess (H and H) grade prior to surgery, location and angiographic features of the VBDAs, endovascular treatment selected, treatment complications, and angiographic and clinical follow-up outcomes. The immediate postoperative, and follow-up digital subtraction angiography (DSA) findings were evaluated by at least two experienced neurointerventionalists to identify the lesion location, the angiographic characteristics of the VBDAs, and the treatment results.
Diagnosis of vertebrobasilar dissecting aneurysms
A computed tomographic angiography (CTA) or a DSA were used to diagnose the VBDAs. The diagnosis of VBDA was made when CTA or DSA revealed vessel irregularity, vessel stenosis/distal narrowing or fusiform dilation, or string sign, or when the DSA showed retention of the contrast medium in the affected vertebral or basilar artery trunk. If the patients were in a nonacute phase, MRI and magnetic resonance angiography (MRA) were used in selected cases to confirm the diagnosis, as they could visualize both the outer surface of the vessel lumen as well as the intraluminal abnormalities. The characteristic diagnostic features of these aneurysms on MRI included the presence of intimal flaps, the double-lumen sign, and intramural hematomas. 
The different management strategies, including internal trapping, stent-assisted coiling, and solely stenting, were selected depending on the features of each lesion [Figure 1] and [Table 1]. All patients first underwent a 4-vessel DSA. Next, the location of the dissecting aneurysm, its collateral blood supply, and the important arterial branches (if involved), were evaluated. When necessary, a balloon occlusion test was used to determine if sufficient collateral circulation would compensate for the loss of blood supply as a result of internal trapping of the vessel harboring the aneurysm. Internal trapping was our first choice if the VBDAs did not involve the dominant vertebral artery (VA) or if any of its important arterial branches such as the posterior inferior cerebellar artery (PICA), anterior inferior cerebellar artery (AICA), or other large perforating arteries, and the collateral blood supply were confirmed to be away from the section of the blood vessel harboring the aneurysm [Figure 2]. The stent-assisted reconstructive techniques, including solely stenting and stent-assisted coiling techniques, were considered if the vessel trapping was not possible. Based on their morphologic presentations, the VBDAs in this study were classified into three subtypes: Aneurysms with lateral protrusion, those causing circumferential enlargement, and those resulting in an atypical dilation [Figure 1]. The circumferential enlargement type referred to a VBDA with a fusiform dilation but without a unidirectional protrusion of the aneurysmal sac; the lateral protrusion type referred to a VBDA with an asymmetrical dilation [Figure 3], [Figure 4] and [Figure 5]; and, the atypical dilation type referred to a VBDA with a sight dilation or an aneurysm without an apparent dilation, or a segment of the vessel lumen that was retaining contrast on DSA [Figure 6] and [Figure 7]. This novel classification, based only on the morphological presentation of aneurysms, without considering the stenosis of the parent artery, proved to be simple and useful in guiding the coil and stent placement. In general, the lateral protrusion type and the circumferential enlargement type needed coil embolization in most cases; whereas, the atypical dilation type often did not have enough space for coiling. The stent-assisted coiling reconstructive technique was selected for lesions with an apparent dilation requiring coiling (there were 5 lesions having the circumferential enlargement, and 21 lesions having the lateral protrusion) [Figure 1]. There were apparent differences in the coiling techniques used for the circumferential enlargement type versus the lateral protrusion type. A stenting procedure preceding the coiling procedure (Technique A) was chosen for the former; whereas, the coiling procedure for the latter was similar to that used in cases with a saccular aneurysm embolization (Technique B). The solely stenting technique was selected if no apparent dilation was found, or only a slight dilation existed (all six lesions with an atypical dilated shape) or if the blood flow was well established by the placement of a single or multiple stent(s) alone, without the need for further coiling (in one lesion with the aneurysm having a lateral protrusion) [Figure 1].
Although all patients were treated as soon as possible after admission to prevent rebleeding, the mean interval time from the onset of hemorrhage to treatment was 4.5 days (range: 1-28 days) because 21 patients were transferred from other hospitals. Endovascular procedures were performed under general anesthesia. All patients received intravenous heparin during the interventional procedure.
Various platinum coils were used to trap the parent artery proximal to the point of the start of its aneurysmal dilation. A minimum of 2-5 mm of the normal vessel wall was embolized with coils proximal to the dissecting artery, if no important arterial branches were involved, to prevent its recanalization [Figure 2]d]. Total occlusion was defined as no contrast medium filling the dissecting vessel on bilateral VA angiogram.
Stent-assisted reconstructive techniques
When the VBDA was diagnosed and the patient was scheduled for reconstructive treatment, antiplatelet medication (300 mg aspirin and 300 mg clopidogrel) was preloaded orally or through a stomach tube 2 h before the procedure. Systemic intravenous heparin was administered in patients who underwent an early embolization to maintain an activated clotting time between 250 and 300s, to prevent an embolic event. Dual antiplatelet agents (75 mg clopidogrel and 100 mg aspirin) were given orally once daily for 6 weeks after the procedure. Following this, 100 mg aspirin was continued for the next 6 months. Self-expanding neurovascular stents were used to reconstruct the dissected artery. If it was possible for the microcatheter to traverse through the first employed stent, overlapping multi-stents were our first choice of treatment, especially when we needed a large radial force to assist in coil occlusion or when we needed low-porosity stents to modify the blood flow and promote thrombosis in aneurysms. Stent(s) placement was aimed at covering the vessel wall at least 5 mm beyond the aneurysm neck (lateral protrusion group); or, extending to the borders of the dissection (in the circumferential enlargement and the slight dilation group) on both the distal and proximal parts of the target vessel. Patients solely treated with stenting mainly had lesions with an atypical dilation, whereas lesions treated with stent-assisted coiling had a circumferential enlargement or the lateral protrusion shape of the vessel wall harboring the dissecting aneurysm [Figure 1]. There were some differences in the technical details between the circumferential enlargement and the lateral protrusion types. For the circumferential enlargement type, we preferred to use stenting followed by the coiling technique (Technique A), described in a previous article by our group.  Thus, a self-expandable stent was navigated into the parent artery without delivering it to the exact site of the aneurysmal sac; then another microcatheter was introduced into the aneurysm sac to deliver the coils. After making a partial occlusion, the stent was delivered to compress the coils against the aneurysmal wall to make the coils within the aneurysmal sac dense and compact. For the lateral protrusion type, we first focused on ensuring the dense embolization of the protruding portion of the VBDAs which were often considered to be the rupture points,;  Following this maneuver, the stent was deployed (Technique B).
Management of arterial stenosis
The VBDAs were often complicated with proximal and/or distal stenosis of the dissecting segment. Balloon dilatation was performed before stenting when the stenosis of more than 75% of the lumen was encoutered [Figure 4]e. Unlike the 6-8 atm used in balloon dilatation for arteriosclerotic stenosis, in our experience, 3-4 atm was usually enough to open the stenosis of intracranial dissecting arteries.
Various types of embolic materials used in the endovascular treatment included detachable coils such as Matrix (Cordis, New Brunswick, New Jersey, USA) and Microplex coils (Microvention, Aliso Viejo, CA, USA); self-expanding neurovascular stents such as Neuroform III (Boston Scientific, Fremont, CA, USA), Leo (Balt, Montmorency, France), Enterprise (Cordis Neurovascular, Miami, Florida, USA), and Solitaire AB (Ev3, Irvine, CA, USA) were used to reconstruct the dissected artery. Gateway percutaneous transluminal angioplasty balloons (Boston Scientific, Natick, Massachusetts) were used to open the stenosis of dissecting arteries.
Serial follow-up angiographic examinations were performed with a conventional DSA to ensure complete angiographic healing and occlusion of the dissected segment. The first follow-up DSA was scheduled at 3-6 months and the second at around 12 months. The patient was then annually followed up with an MRA or a CTA. The patient outcome was measured using the modified Rankin Scale (mRS) score through neurologic examination at follow up visits or by assessing his/her neurological status during a telephonic interview.
The baseline demographics, procedural complications, angiographic results, and clinical results were retrospectively analyzed.
Clinical and imaging characteristics
Thirty men and 10 women with a mean age of 48.0 years (range: 25-64 years) were selected for this study. The basilar artery was involved in six patients, four with only the basilar artery and the other two with the involvement of the vertebrobasilar artery. In the 34 VA dissections without basilar involvement, the dissections were proximal to the PICA in seven patients, distal to it in 12, and involved the origin of the PICA in 14; the PICA could not be identified in one patient. The severity of clinical manifestations was rated as H and H Grade I (n = 24, 60%), Grade II (n = 9, 22.5%), Grade III (n = 6, 15%), and Grade IV (n = 1, 2.5%).
Results of first operation
Seven patients were treated with internal trapping, 26 with stent(s)-assisted coiling, and 7 with solely stenting [Table 1]. All seven patients treated with internal trapping had total occlusion without any operation-related complications.
Of the 26 patients treated with stent(s)-assisted coiling, one patient who had a basilar artery dissecting aneurysm suffered an acute in-stent thrombosis during surgery. Fortunately, the basilar artery was recanalized by an immediate intra-arterial thrombolysis with 300,000 IU urokinase, which prevented deterioration of the patient's condition [Figure 5]. The other 25 patients treated with a single or multiple stent-assisted coiling had no operation-related complication.
Among the seven patients treated solely with stenting, five aneurysms got obliterated and 2 aneurysms had further retention of contrast after the stent deployment. There were no complications during surgery.
Results of postoperative outcomes and the first follow-up
Thirty-eight patients had their first follow-up angiography at 3-7 months (median 5.2 months) after treatment. Two patients (1 died of rebleeding; and, the other, who had a H and H Grade IV before surgery, developed a persistent vegetative state after surgery although the operation was successfully performed) did not undergo an angiography.
All seven patients treated with internal trapping had a satisfactory outcome; none experienced rebleeding, recanalization, or an ischemic episode after the treatment.
Of the 26 patients treated with stent -assisted coiling, 1 suffered hemiparesis after the operation because of a small cerebral cortical infarction. His motor function partially recovered and he persisted with an mRS score of 1 after 6 months. One patient suffered a small rebleed on the fifth day after the endovascular intervention but did not have another recurrence after conservative management. His follow-up DSA at the third month showed that the aneurysm had got obliterated. One patient had recanalization at the third month of follow-up and underwent a second procedure of stent implantation; at the 14-month follow-up, the aneurysm had disappeared. Another patient developed a small remote cerebellar hemorrhage, which was not directly related to the aneurysm. This occurred on the second day after the operation for which he received conservative treatment; he was discharged 8 days later without further hemorrhage. A follow-up DSA at 6 months showed that the aneurysm was cured. One patient, who had an H and H Grade IV before the intervention, developed a persistent vegetative state after the procedure and did not receive any follow-up angiography. The other 21 patients did not have any rebleeding, recanalization, or ischemic events after treatment.
Of the seven patients treated solely with stenting, 1 suffered rebleeding on the eighth day and died on the ninth day after the procedure because of brain stem infarction. One patient suffered a small area of rebleeding on the third day after surgery and received conservative treatment; he recovered well without any recurrence of rebleeding. His follow-up DSA at the third month showed that the aneurysm was cured. Another patient [Figure 7] had recanalization of his aneurysm that was noticed at the 7-month follow-up. He received a repeat treatment with stent-assisted coiling and was awaiting his next follow-up DSA. The other four patients did not have any rebleeding, recanalization, or ischemic events after the interventional procedure.
Results of the last clinical follow-up
Clinical follow-up was available in 39 cases that ranged from 6-30 months (median 12.9 months) except in one patient who died of rebleeding. Of the 40 cases of VBDA available at follow up, 30 were ranked as mRS Grade 0, 8 as Grade 1, 1 as Grade 4, and 1 as Grade 6.
VBDAs are being increasingly recognized as a source of SAH, , and endovascular approaches have become major therapeutic options for VBDAs. , However, the endovascular strategies for ruptured VBDAs remain controversial and little is known about the mid-term or long-term results of the endovascular treatment of VBDAs. In this report, we study the results and clinical outcomes of 40 consecutive patients with ruptured VBDAs. Our therapeutic strategy is based on a novel morphological classification of ruptured VBDAs into three subtypes.
This classification has proven to be helpful in the selection of treatment strategies [Figure 1]. Takagi et al.,  had previously classified VA dissecting aneurysms into seven types, based on the patterns of dilation and stenosis of the VA. These included the following: (A) Double-lumen; (B) fusiform; (C) lateral protrusion; (D) string; (E) proximal stenosis and distal dilation; (F) proximal dilation and distal stenosis; or (G) occlusion. This classification was not as helpful in guiding therapeutic intervention. It is also difficult to practically apply it in therapeutic practice. In fact, VBDAs showing a string sign (tapered narrowing) or an occlusion on DSA seldom ruptured, and VBDAs with a double-lumen sign on DSA were rarely observed. , Our classification of these aneurysms into the three sub-types depends mainly on the aneurysmal configurations, without taking into consideration the parent artery stenosis. It is effective in guiding the therapeutic intervention for ruptured VBDAs [Figure 1].
The endovascular parent artery occlusion mainly included proximal arterial occlusion as well as internal trapping. None of the patients in this series were treated with solely a proximal arterial occlusion because we considered this technique to be unable to protect against rebleeding due to retrograde flow of blood to the dissected segment.  Selected cases treated with internal trapping usually achieve good results.  In the present series, there were only seven patients chosen for this method because of the selection bias of the patients hospitalized. Our hospital receives several patients with severe cerebrovascular diseases from all over North China. Many VBDAs patients received the trapping operation in primary hospitals. Many of the patients transferred to our centre had an associated complex neurological status and required stent-assisted therapy. Rest of the 33 patients in our cases series either had lesions that involved the dominant VA, PICA or AICA, or had an insufficient collateral blood supply after parent artery occlusion. Thus, they were not suitable candidates for internal trapping. In this situation, a high-flow bypass has been reported to be a good solution.  However, the high-flow bypass was not adopted in recent years in our institute because the location of dissection makes the surgical approach technically demanding with a high risk of cranial nerve damage.  Hence, we chose the alternative approach of stent-assisted reconstructive technique when the parent artery could not be occluded. Nevertheless, internal trapping is still the most reliable treatment option when the parent artery can be sacrificed.
With the ongoing development of interventional devices, stent-assisted reconstructive techniques for acute ruptured dissecting aneurysms are emerging as promising options. , A stent may prevent rebleeding in the acute stage by repositioning the split intimae, by redirecting the blood flow, and by reducing the stress on the walls of a dissecting aneurysm.  In our study, of the seven patients treated with this technique, 1 had recanalization and 2 suffered from rebleeding. This outcome was less satisfactory than that reported by Jiang et al., who treated 2 ruptured basilar artery dissections with stents alone and had no complications.  However, in the report by Kim et al., one patient with a ruptured dissection was treated with stents alone but suffered from rebleeding.  Our own results and that of Kim et al., suggest that the stent-alone option is not safe for sufficient addressal of a ruptured VBDAs.
Flow-diverter devices such as the Silk (Balt Extrusion, Montmorency, France) and Pipeline Embolization Device (PED; Ev3, Irvine, CA) were reported as useful tools to treat VBDAs without aggravating the mass effect. ,, Reports of treating ruptured VBDAs with flow-diverter devices are scarce. ,, Narata et al., reported on two ruptured VA dissections treated with the PED. Within 3 months, complete occlusion was achieved in both the cases with no procedural morbidity or rebleeding.  These devices were not used in our study because both the US Food and Drug Administration and the China Food and Drug Administration have not yet approved their application in posterior cerebral circulation. The flow-diverter devices were designed to treat patients with complex and recurrent aneurysms. When intracranial aneurysms are treated with flow-diverter devices, the problems encountered include the occurrence of a delayed hemorrhage as well as the compromise of patency of the perforating arteries and the side branches that got covered by the device.  Although the flow diverter devices have shown some promise in the treatment of ruptured VBDAs, these devices need further study.
In most of our cases (26 of 40), the stent-assisted coiling technique was used because it not only maintains the patency of the parent artery, but also reinforces the site of the aneurysmal rupture as much as possible. Special emphasis was undertaken to ensure a dense packing of the embolization material into the most dilated portions of the VBDAs, as these areas were considered to be the potential rupture points.  The outcome of patients treated with stent-assisted coiling was better than that seen after the stent-alone technique, but worse than that seen after internal trapping [Table 1]. The stent-assisted coiling technique did not eliminate the mass effect of the dissecting aneurysms, which might limit its application while treating giant VBDAs. In this series, all patients suffered from an aneurysmal SAH that was not associated with any mass effect. The series also did not have any giant VBDAs. Further study is needed to investigate the safety of stent-assisted coiling in VBDAs with mass effect.
We used balloon dilatation of the stenosed artery harboring the dissecting aneurysm in one particular case as shown in [Figure 4]. The patient, who had recurrent SAH in one week and also suffered from transient apnea, needed an emergency operation. At first, we tried papaverine injection through the catheter to open the arterial stenosis, but this strategy failed. Then, we adopted the balloon dilatation technique and achieved a good result. Our main consideration for this technique was based on the following two points: (1) We were apprehensive that the radial strength of intracranial self-expanding stents was not adequate to effectively dilate the arterial stenosis, thereby increasing the risk of stent thrombosis; (2) We were also expecting the balloon dilatation of the stenosed artery to reposition the split intimae and contribute to vascular repair. This technique originated from our experience in interventional therapy. This vessel dilatation strategy can be an alternative method after careful consideration of the vessel characteristics in particular cases.
This series has limitations of being retrospective in nature, with a patient selection bias, and inclusion of a limited number of cases from a single center.
The mid-term and long-term follow-up in this study confirmed the efficacy of the endovascular treatment for ruptured VBDAs. The treatment protocol for ruptured VBDAs proposed in this study proved to be simple and useful.
Financial support and sponsorship
This work was supported by the National Natural Science Foundation of China (Grant Numbers 81301003, 81171079, 81371315, and 81220108007) and by the Special Research Project for Capital Health Development (Grant Number 2014-1-1071).
Conflicts of interest
There are no conflicts of interest.
[Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7]