Open access peer-reviewed chapter
Abstract
Treatment strategies for cerebral aneurysms have changed dramatically in recent years with advances in endovascular therapy. Advances in devices, endovascular surgeons’ skills, and diagnostic modalities have improved the results of endovascular treatment, making it a safer and more reliable treatment option. On the other hand, we are encountering an increasing number of cases of postoperative recurrence. Direct surgery has a specific role in treating these recurrent cases, and it has become essential to establish a decision-making method and surgical technique for treating these cases. In this chapter, I will discuss the treatment options for recurrent cerebral aneurysms after endovascular treatment and the practical application of directclipping and bypass surgery.
Keywords
- cerebral aneurysms
- direct surgery
- endovascular treatment
- recurrence
- neurosurgery
1. Introduction
Direct surgery for recurrent cerebral aneurysms after endovascular treatment is complicated, and great care must be taken in determining its indications. In addition, the actual procedure often requires technical ingenuity. In this chapter, we will discuss in detail the role of direct surgery for this aneurysm and its surgical innovations.
2. History of treatment for intracranial aneurysms
The history of craniotomy clipping for cerebral aneurysms is long. Dandy WE reported clipping surgery using a V-shaped malleable clip in 1937 [1]. Many papers have been published since 1959 when Mount LA et al. reported a procedure using the highly operable Selverstone clamp [2]. Since then, craniotomy clipping results have improved with the advent of the latest cerebral aneurysm clips and surgeon skill improvements. Many neurosurgeons have accepted this as a highly reliable long-term procedure with a low recurrence rate for unruptured and ruptured cerebral aneurysms [3, 4, 5]. The most significant advantage of this treatment is that it immediately removes the cerebral aneurysm from the general circulatory system, leading to a very low probability of rupture or rerupture. On the other hand, it is necessarily a relatively invasive procedure because it involves skin and muscle incisions, craniotomy, and subdural brain manipulation, making it a burdensome procedure for patients with medical complications and the elderly. Minimally invasive surgical techniques centered on key hole surgery have been developed to solve this problem, and patient satisfaction has improved, and it has also been reported to reduce the frequency of cerebral vasospasm in subarachnoid hemorrhage cases and to improve treatment prognosis [6, 7, 8, 9].
Endovascular treatment as a counterpart to cranial clipping as a treatment for cerebral aneurysms was reported as early as 1832. It was intended to occlude the aneurysm by wire insertion or electrothrombosis. Still, it was not used to occlude intracranial arteries. The most significant disadvantages of endovascular treatment are its high rate of complications such as distal embolism, high mortality rate, and the long time required for occlusion [10]. Subsequently, treatment of large and giant cavernous sinus internal carotid artery aneurysms using a detachable balloon was reported by Serbienko and colleagues. Since then, many good treatment results have been reported with improvements and performance enhancements by Romadanov, Debrun, Hieshima, and Taki [11, 12, 13, 14]. Conversely, they are challenging to apply to intradural cerebral aneurysms and new devices have been awaited.
Endovascular treatment of cerebral aneurysms has made great strides since the introduction of the Guglielmi Detachable Coil (GDC) in 1991 [15]. Compared to conventional devices, this is an electrically detachable platinum coil, easy to operate, and incredibly soft, making it less invasive to the aneurysm wall, enabling safer and more reliable endovascular treatment of intracranial aneurysms. The GDC received FDA approval in 1995. Since then, the GDC has become a widely used treatment for cerebral aneurysms. The International Subarachnoid Aneurysm Trial (ISAT), a randomized controlled trial of coil embolization versus surgical clipping for ruptured cerebral arterial aneurysms, was published in 2002 [16]. The results showed that in patients in whom endovascular coiling and neurosurgical clipping were the treatment of choice for ruptured intracranial aneurysms, the 1-year disability-free survival rate was significantly better with endovascular coiling. The long-term risk of rebleeding from treated aneurysms was also lower for both treatment modalities but was suggested to be slightly more frequent with endovascular coiling [16]. Since the publication of this report, coil embolization has become a more aggressive option for ruptured and unruptured cerebral aneurysms, especially in Europe and the United States. Furthermore, the Barrow Ruptured Aneurysm Trial (BRAT), which compared coil embolization and surgical clipping to treat ruptured cerebral aneurysms, confirmed that the treatment prognoses for both procedures were comparable [17, 18]. In a report from Australia covering cases from 2008 to 2018 based on the Australian National Hospital Morbidity database, endovascular treatment for cerebral aneurysms accounted for 58.4% of all cases [19]. Furthermore, the Nationwide Inpatient Sample database from 2002 to 2012 reported that in a total of 23,053 patients with unruptured cerebral aneurysms, coil embolization was the procedure of choice in approximately 73% of cases [20]. Opportunities for endovascular treatment options for cerebral aneurysms, coupled with advances in the technology of the devices and surgeons, will continue to increase in proportion.
3. The aneurysmal recurrence rate after endovascular coil embolization has improved but is still high
While endovascular treatment is a minimally invasive treatment for cerebral aneurysms, the biggest problem is that, unlike craniotomy clipping, which is a treatment that can completely exclude cerebral aneurysms from the circulatory system, it is a method of filling coils with aneurysms while they are still in the circulatory system, which inevitably results in a relatively high postoperative recurrence rate. According to the ISAT results, the cerebral aneurysm recurrence rate after endovascular treatment is reported to be 17.4% [16]. The BRAT results also reported a 15.6% cerebral aneurysm recurrence rate after 1 year of endovascular treatment [21]. According to reports on so-called real-world data from other than these randomized controlled trials, the recurrence rate is 20–30% [22, 23]. But recent reports indicate that the rate of cerebral aneurysm recurrence after endovascular treatment is trending downward, from 10% to the 5% range [24, 25]. This is primarily due to new technological innovations such as stent-assisted coil embolization. On the other hand, as mentioned above, the number of cerebral aneurysms treated endovascularly is increasing. As the population grows, it is clear that the number of aneurysms requiring retreatment will inevitably increase, no matter how low the recurrence rate becomes.
4. The rupture rate of recurrent aneurysms after endovascular coil embolization is low. What are the characteristics of the recurrence with a high risk of rupture?
The rupture rate of recurrent aneurysms after endovascular coil embolization is low. A systematic review by Arnaout OM et al. reported the risk of recurrent cerebral aneurysms after initial coil embolization of 2.3 to 8.3% or 0.8% per year [22]. A study by the CARAT Investigators of 1010 patients (299 after coil embolization) reported that the rate of delayed rebleeding from the recurrent aneurysm after coil embolization was 0.11% per year [26]. As these indicate, the risk of rupture of recurrent cerebral aneurysms after initial coil embolization is low. Thus, these are relatively stable lesions, and not all are indications of retreatment.
On the other hand, we have experienced cases of death or serious illness due to the rupture of these recurrent cerebral aneurysms, and we would like to call for caution.
We present a case of our own experience (Figure 1). The patient was a 63-year-old woman with a subarachnoid hemorrhage due to a ruptured basilar bifurcation aneurysm and underwent coil embolization at another hospital 3 years earlier. She was discharged home with a modified Rankin Scale score (mRS) of 0. During outpatient follow-up, a recurrence of the aneurysm, which had been treated for 3 years, was found, and the patient was referred to our outpatient clinic. Her neurological imaging study showed marked re-enlargement of the aneurysm due to coil compaction (Figure 1a and b), and we were considering coil embolization for retreatment of the aneurysm. However, 1 week after the visit, she suddenly developed a loss of consciousness and was brought into our emergency department. When she came to our hospital, she was in a coma with bilateral dilated pupils, and a head CT scan showed marked intraventricular hemorrhage and acute hydrocephalus (Figure 1c). She underwent emergency ventricular drainage, but the neurological findings did not improve even after the operation, and she died and was discharged from the hospital the day after arrival.
Figure 1.
(a)-(c), (a): Lateral view of a plain X-ray image of the head: The coil mass is divided into two pieces due to coil compaction. (b): Magnectin resonance imaging (MRI) coronal section of the head shows the recurrent partially thrombosed basilar bifurcation aneurysm. (c): A head computed tomography (CT) scan shows marked intraventricular hemorrhage and ventricular dilatation.
As this case demonstrates, clinicians must be fully aware of the possibility of recurrent cerebral aneurysms that can rupture and cause death or serious clinical consequences. So what are the characteristics of recurrent cerebral aneurysms are most likely to lead to rupture?
What are the characteristics of recurrent cerebral aneurysms after endovascular treatment with a high risk of bleeding?
It has been reported that progressive growing aneurysms are at high risk for hemorrhage [27].
The rebleeding rate of cerebral aneurysms with recurrent filling is reported to be 7.9% over 5 years [28].
Recurrent aneurysms with fundal migration of coil loops mean a dynamic inflammatory process is involved, and a high bleeding rate has been reported [29].
A high rebleeding rate of 17.6% has been reported when the occlusion rate after coil embolization is less than 70% [26]. In such recurrent cerebral aneurysms after coil embolization, as described above, the risk of severe subarachnoid hemorrhage due to bleeding is considered high. Thus, aggressive treatment should be recommended in these cases.
5. Role of direct surgery for recurrent aneurysms after endovascular coil embolization
The treatment selection for recurrent cerebral aneurysms after endovascular treatment should be based on an individualization policy. However, the difficulty of direct surgery is high in these aneurysms because of coil mass extrusion, thrombus formation in the aneurysms, adhesion to vital cranial nerves and branches due to inflammatory changes in the aneurysm wall, thickening of the aneurysm wall, and coil loop scarring to the parent artery. On the other hand, endovascular treatment is often relatively easy to retreat. Therefore, endovascular retreatment is the first choice to treat recurrent cerebral aneurysms after endovascular treatment safely.
Is endovascular treatment the optimal retreatment strategy for all patients with recurrent cerebral aneurysms after endovascular treatment? The recurrence rate of cerebral aneurysms after initial endovascular treatment has been reported to range from 4.7 to 17.4% [30, 31, 32]. On the other hand, the re-recurrence rate of endovascular retreated recurrent aneurysms has been reported to have a high cerebral aneurysm recurrence rate ranging from 44.1 to 48.8% [32, 33, 34]. Therefore, if endovascular retreatment is chosen for all post-endovascular recurrent cerebral aneurysms, the reoccurrence rate will inevitably be high, and multiple retreatments may sometimes be required. Although endovascular retreatment is a relatively safe and easy treatment for recurrent cerebral aneurysms after initial endovascular treatment, we should be careful not to choose this treatment method too easily.
It has been reported that the recurrence rate of endovascular treatment of recurrent cerebral aneurysms after initial endovascular treatment varies greatly depending on the mechanisms of recurrence (Figure 2). When endovascular treatment was selected for recurrent cerebral aneurysms after initial endovascular treatment, the multiple re-coiling rates for patients with recurrence by the coil compaction mechanism was 21.3%. The multiple re-coiling rates for patients with recurrence by the regrowth mechanism were extremely high at 85.7% [29]. Therefore, choosing direct surgery for recurrent cerebral aneurysms with a regrowth mechanism is crucial to minimize the multiple recurrences.
Figure 2.
(a)-(d): Schema of the mechanisms of the recurrence. (a): Complete obliteration of the aneurysm. (b): Coil compaction. (c): Aneurysm regrowth. (d): Fundal migration.
In addition, the flow diverter is now available as a new option for treating recurrent cerebral aneurysms after initial coil embolization. In a study comparing the pipeline embolization device (PED: 18 patients) and coil embolization for recurrent aneurysms after initial coil embolization, the complication rate was similar for PED and coil embolization, and the recurrence rate was significantly lower for PED than for coil embolization (p < 0.037) [35]. Moreover, in a study of flow diverter treatment (17 patients) for recurrent aneurysms after initial coil embolization with the stent, all patients had good outcomes (mRS 0-2), 16 patients had complete aneurysm occlusion, and one patient tended aneurysm regrowth [36]. Thus, the flow diverter, a novel treatment method, is currently a promising treatment option for recurrent cerebral aneurysms after initial coil embolization. Future case series and long-term follow-up studies are warranted.
In deciding the optimal treatment for patients with recurrent cerebral aneurysms after initial coil embolization, it is critical to consider the presence or absence of systemic complications comprehensively, the site of the aneurysms, and the mechanism of aneurysm recurrence in each case to determine the optimal treatment strategy.
6. Tips of direct surgery for recurrent aneurysms after endovascular coil embolization
When choosing open clipping of a recurrent cerebral aneurysm after initial coil embolization, it is critical to confirm by preoperative cerebral angiography that there is sufficient space between the neck and the coil mass to allow for clip application. (Figure 3a and b) Toyota et al. reported that a remnant neck height of the aneurysm more significant than 2 mm is a prerequisite for surgery if the coil mass within the aneurysm is not removed [37]. Also, Waldron et al. reported that open cerebral aneurysm clipping without removing the coil mass in the aneurysm is unsuitable when the coil width and compaction height ratio exceeds 2.5 and a wedge angle greater than 90 degrees [38]. Confirming these findings by preoperative cerebral angiography is essential.
Figure 3.
(a) and (b): Schema of the morphological parameters of recurrent aneurysms after endovascular coil embolization. (a): The gray two-direction arrow indicates a coil width (C), and the black two-direction arrow indicates either a compaction height (H) or a remnant neck width (RNH). (b): The angle shown in the figure indicates a wedge angle. Aneurysms with RNH greater than 2 mm or a C/H ratio greater than 2.5 with a wedge angle greater than 90 degrees are unsuitable for direct clipping surgery without coil removal.
Perioperative stroke complications have been reported to be higher in patients undergoing intraoperative coil mass extraction [23]. Coil extraction was performed in 3/111 patients (2.7%), all of whom suffered a postoperative stroke [39]. The effects of coil embolization of cerebral aneurysms on the vital structure of the aneurysm, mother vessel, branches, and cranial nerves have been attributed to inflammatory and degenerative change mechanisms. A coil mass within the aneurysm causes inflammation and degeneration, resulting in extrusion of the coil mass outside the aneurysm, invasion of the surrounding vital structure, inflammatory adhesions, protrusion of the coil loop into the mother vessel, and scarring of the vessel wall. Surgical coil mass extraction in this condition is likely to cause steno-occlusion of the parent artery and damage to the vital structure. These can lead to postoperative stroke and neurological sequelae. Therefore, in the case of open clipping of recurrent cerebral aneurysms after initial coil embolization, coil mass extraction should be avoided as much as possible to ensure a safe procedure with a low rate of surgical complications.
Even in cases where preoperative imaging has shown sufficient space for clip application in the recurrent cerebral aneurysm, intraoperative findings may indicate that the room is smaller than expected during surgery. This phenomenon may be due to thrombus formation caused by coil mass in the aneurysm or thickening of the aneurysm wall due to inflammatory changes. In addition, a coil loop in the neck of the aneurysm may prevent complete occlusion of the neck when a single clip is applied (Figure 4a). The tandem clipping method has been reported to help deal with incomplete occlusion of cerebral clips due to stiff neck aneurysm walls and coil loops (Figure 4b) [40]. In this technique, a fenestrated aneurysm clip is applied to the far side aneurysm neck, skipping the near side aneurysm neck, and an additional clip is used to close the near side aneurysm neck. This technique is beneficial in narrow aneurysm neck spaces, stiff aneurysm neck walls, and the presence of coil loops in the neck, as complete occlusion of the aneurysm neck can be achieved without coil mass extraction. On the other hand, for large or giant cerebral aneurysms that recur after initial coil embolization and are at high risk for open aneurysm clipping, mother vessel occlusion with intracranial or extracranial bypass may be helpful [38, 40]. By this surgical strategy, direct manipulation of the aneurysm is no longer necessary, and it can be a safe treatment for recurrent cerebral aneurysms after coil embolization of deep locations like the upper basilar artery system or when there is already a high mass effect on the vital structures.
Figure 4.
a (upper) and b (lower): Schema of the neck clipping of the recurrence. (a): When a single aneurysm clip is applied to the aneurysm neck, atherosclerotic or inflammatory wall thickening (small black arrow) and coil loop inside (small white arrows) often prevent complete closure of the neck (thick white arrow). (b): The tandem clipping method, in which a fenestrated aneurysm clip is applied to the far side aneurysm neck, skipping the near side aneurysm neck, and an additional clip is used to close the near side aneurysm neck, is extremely useful in the above situation, as it provides complete closure of the neck.
7. Illustrative case presentations
Figure 5.
a-c: The imaging studies of illustrative case 1. (a): Follow-up DSA (lateral view of right ICGA) 6 months after initial coil embolization showed remarkable recurrence of the treated IC-Pcom aneurysm (white arrow). (b) and (c): Postoperative plain CT and CT angiography showed no complication and complete obliteration of the aneurysm.
Postoperative CT showed no complication and complete obliteration of the aneurysm (Figure 5b and c). Her postoperative course was uneventful, and she was discharged home without a neurological deficit.
Figure 6.
a-c the imaging studies of illustrative case 2. (a) Follow-up DSA (lateral view of right ICGA) 41 months after initial coil embolization showed remarkable recurrence of the treated IC-Pcom aneurysm (white arrow). (b) and (c) postoperative plain CT and CT angiography showed thin epidural hematoma and complete aneurysm obliteration.
Intraoperative findings (
Postoperative CT showed a thin epidural hematoma and complete aneurysm obliteration (Figure 6b and c). Her postoperative course was uneventful, and she was discharged home without a neurological deficit.
Figure 7.
a-f: The preoperative (a-c) and postoperative (d-f) imaging studies of illustrative case 3. (a) Silent MRA 30 months after the second treatment. (b) T1-weighted MRI. (c) 3D rotational angiography. The imaging studies showed recurrent partially thrombosed giant left IC-Pcom aneurysm (white arrow). (d) Postoperative diffusion-weighted MRI. (e) and (f): Postoperative DSA anterior-posterior and lateral view. The imaging studies showed no ischemic complication and complete aneurysm obliteration with preservation of normal arteries.
Intraoperative findings (Video 3 https://1drv.ms/v/s!AnNEb0cDd-ygmSsspZ6yOvo4Mle1?e=hlee0e): The stent was inserted in the left proximal intracranial ICA, but proximal control at this site was confirmed feasible. Left Pcom origin was observed at the proximal neck of the aneurysm. Coil mass inside the aneurysm dome and stent strut were seen through the wall of the dome and ICA. The left anterior choroidal artery and perforators from Pcom firmly adhered to the dome of the aneurysm. The adhesion was detached with sharp dissection. While performing temporary occlusion in the proximal intracranial ICA, first, we applied a fenestrated titanium clip in partial occlusion of the far side aneurysm neck. ICG-VA revealed the residual flow into the aneurysm through the near side of the neck of the aneurysm. We added a straight titanium clip in a parallel fashion to secure the complete obliteration of the aneurysm. ICG-VA showed complete obliteration of the aneurysm and preservation of the parent artery and branches.
Postoperative imaging studies showed complete aneurysm obliteration without complication (Figure 7d–f). His postoperative course was uneventful, and he was discharged home without a neurological deficit.
8. Conclusions
The role of craniotomy in treating recurrent cerebral aneurysms after initial coil embolization has been discussed in detail. The optimal treatment strategy for this lesion should be decided based on the location of the aneurysm, the mechanism of recurrence, the presence or absence of systemic complications, and the performance status of the individual patient. In the case of recurrence by aneurysmal regrowth mechanisms, the choice of direct surgery leads to a low recurrence rate. In direct surgery, clipping without coil mass extraction is safer. The tandem clipping method is a beneficial technique that can achieve complete occlusion of these aneurysms.
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