Surgical treatment of intracranial aneurysm recurrence after clipping

Overview

Recurrence of intracranial aneurysms (IA) after surgical treatment (aneurysm clipping) is relatively rare in clinical practice. The treatment of such an aneurysm requires an individualized approach based on precise medical imaging and experience of the team. Surgical treatment of recurrent aneurysms is technically more demanding compared to primary surgery especially due to postoperative changes. The goal of this study is to review current knowledge and management of recurrent IA after clipping and present our experience with such cases.

Keywords:

intracranial aneurysm – clip – cerebral angiography – medical imaging

This is an unauthorised machine translation into English made using the DeepL Translate Pro translator. The editors do not guarantee that the content of the article corresponds fully to the original language version.

 

Introduction

Brain aneurysms were first surgically treated in 1931 by Norman Dot in Edinburgh, who wrapped a ruptured aneurysm of the left middle cerebral artery from the subfrontal approach in Colin Black, whose operation was preceded by three ruptures of this aneurysm. The first aneurysm clipping was then performed by Walter Dandy in 1937 for a ruptured aneurysm of the posterior communicating artery. The introduction of the microscope into neurosurgical surgery in the 1960s contributed significantly to further developments. Continued advances in surgical treatment have meant the development of ever smaller and more delicate instruments, temporary clips, improved diagnostic techniques, perioperative diagnostic methods such as perioperative videoangiography (VAG) using indocyanine green (ICG), or reduced use of perioperative flaps to reduce manipulation of brain tissue and increase surgical safety.

However, after the publication of the International Subarachnoid Aneurysm Trial (ISAT), there has been a partial shift in the treatment of intracranial aneurysms (IA) from surgery to endovascular therapy [1]. On the other hand, the medium- and long-term results of international studies in the following years have shown an increased recurrence rate of endovascularly treated IAs compared to those treated surgically [2,3]. Thus, the advantage of surgery is, among other things, the long-term stability of aneurysms treated in this way. Therefore, current recommendations prefer, among other things, surgical treatment in e.g. young patients (< 40 years) due to life expectancy [4,5]. On the other hand, it should be noted that even in the most experienced hands, aneurysm clipping has a 7% risk that the aneurysm will not be completely resolved after 10 years [3]. Therefore, in practice, we must necessarily encounter a patient with recurrence of IA after clipping. In this paper, we focus on the care of patients after surgical treatment of IA.

Historical development

The first documented case of aneurysm recurrence was probably described in 1965 [6]. The patient died of a left middle cerebral artery aneurysm rupture after previous treatment of aneurysm rupture with a tantalum clip of the right middle cerebral artery 11 years earlier. The autopsy then confirmed a 14 × 11 multilobulated recurrence of the middle cerebral artery aneurysm. In the 1980s, there was a view that the risk of rupture in a patient with a residual aneurysm was very low and therefore, according to Feuerberg et al, there was no reason to reoperate such a patient [7]. On the other hand, in 1984, Drake et al. described a series of 115 reoperated IA recurrences [8]. They also described several reasons for their incomplete treatment and developed the first simple classification (Figure 1). In 36% (41/115) of the patients, a new neurological deficit developed, either due to bleeding or to expansive sac behavior.

Other studies, mostly from the 1990s, have shown that the annual risk of bleeding from aneurysm remnant is 1.9%, which is higher than that of most unruptured aneurysms [9]. The Cerebral Aneurysm Rerupture After Treatment (CARAT) study confirmed that the risk of bleeding is directly proportional to the size of the sac remnant [10]. In the cohort of surgically or endovascularly treated ruptured IAs in the CARAT study, the 4-year risk of rerupture for primary completely obliterated aneurysms was 1.1%, whereas for aneurysms with a residual of more than 70% it was 17.6%. According to another study, 3.5-15% of residual aneurysms grow and 28% of them then undergo rerupture [11].

Residual aneurysm after clipping

Leaving an aneurysm residue may be the result of a technical error or imperfection in the aneurysm clipping or it may be a purposeful step of the surgeon determined by the anatomical conditions in the vicinity of the sac. The reason for leaving the aneurysm remnant is most often the detachment of one or more branches from the neck or sac of the aneurysm (Figure 2). Attempting to completely close the IA sac would otherwise lead to obliteration of the arterial branch with possible development of ischemic neurological deficit. The rest of the sac can then be reduced by coagulation and wrapped with e.g. fascia or Gore-Tex (wrapping), or by securing the wrap with a clip [12]. On the other hand, the residual sac may be left unintentionally. A frequent cause of this is a confusing situation in patients with a ruptured aneurysm in the setting of massive subarachnoid haemorrhage in combination with e.g. cerebral oedema. Another cause may be complex anatomical conditions, e.g. in aneurysms of the anterior communicating artery or basilar apex, which do not allow a 360° view of the sac and its neck. Even clip deployment with complete occultation of the sac may not mean 100% resolution of the aneurysm, as less force in the distal part of the clip, e.g., in atherosclerosis or neck calcification, may cause imperfect closure of the sac with persistent blood flow to the aneurysm (Figure 3). Therefore, complete closure of the aneurysm sac should also be checked after clip loading using adjuvant methods such as perioperative VAG or perioperative direct dopplerometry. If technically feasible, we recommend to cut the sac perioperatively to verify the occlusion. Similarly, we verify that no flow stenosis or even occlusion of any of the arterial branches has occurred with the clip. Flowmetry using Charbel probes can be used for this purpose in addition to these methods. The optimal solution is then to use intraoperative DSA, where a full radiological evaluation of the treated aneurysm can be performed within 15 min before the bone plate is returned.

As early as 1967, Drake described the risk of recurrent bleeding in three groups of patients according to his classification; those with complete sac occlusion (45 patients), those with a small remnant (12 patients) and those with most or all of the sac left (13 patients). In patients with complete pouch occlusion, the authors observed no recurrence of bleeding (0%), while in patients with lesser residual pouch, they observed two early and two late bleeding from the pouch (33%), resulting in the death of three patients. Of course, the worst results were in group 3, where the authors observed four early and three late bleeds (54%), resulting in six deaths.

Several more recent studies have shown that using postoperative DSA, a residual sac can be found in 2.3-16% of cases [13-15]. For example, a 1998-2001 study of clipped aneurysms from Helsinki, one of the most respected centers for cerebral aneurysm surgery in the world, showed that residual aneurysm after clipping was diagnosed in 12% of patients. In a risk analysis, the authors then found that patients with ruptured aneurysms (14 vs. 9%), posterior basin aneurysms, and large or giant aneurysms had a higher risk of leaving a residual.

Ito et al. evaluated 244 clipped patients and diagnosed incomplete clipping treatment in six of them (2.5%). Two of these patients had an early rerupture within 30 days; fortunately, in only one patient did the rerupture lead to a worsening of the clinical condition. Four patients (1.6%) underwent reoperation. Five patients had aneurysms of the anterior communicating artery complex and one patient had an aneurysm of the arteria basilaris. The authors evaluated the causes of insufficiently clipped aneurysms, and in four cases it was insufficient aneurysm clearance during surgery, in one case it was insufficient ability of the clip to close the thick wall of the neck of the aneurysm, and in one case it was a residual between the branches of the aneurysm clip.

Radiological evaluation after primary surgical treatment of aneurysm

We define an aneurysm residual as an incompletely treated IA with a leftover sac or neck. Previously, it was common practice for surgeons to rely on perioperative findings to assess the completeness of IA treatment without the need for postoperative radiological imaging. Also at our institution, until approximately 2007, we standardly indicated only a native CT scan of the brain on postoperative day 1 to rule out complications (ischemia, hemorrhage, contusion). However, there is an increasing emphasis on objectifying the completeness of the treatment of the brain aneurysm, i.e. performing imaging after surgical treatment of the aneurysm, either by CTA or DSA. Therefore, since 2007, we have been performing CT scans for all aneurysms as standard, incl. CTA of the cerebral arteries (Fig. 3). This is even if we cut the aneurysm sac or verify the completeness of the clip by a combination of perioperative transcranial Doppler and ICG. According to our experience, 1 time we observed an unexpected residual aneurysm, which was related to insufficient clip strength in the distal part (which is the weakest part of the clip). Despite our impression of the operation, the aneurysm was inadequately treated, which was resolved the following day by deploying a parallel clip distal to the original aneurysm with complete resolution of the aneurysm.

The literature shows that if complete aneurysm repair was confirmed immediately after the procedure by 3D angiography, the risk of recurrence is close to 0% [16]. On the other hand, the risk of recurrence of incompletely resolved aneurysms was 11.8% less than 4 years after the primary operation. Thus, complete treatment of the aneurysm sac is an absolutely crucial influential factor in the prevention of IA recurrence.

Recurrence of aneurysm after clipping

The efficacy of surgical treatment of aneurysms is high, with an annual risk of recurrence of 0.26-0.53% [9,17-19]. Significant risk factors for IA recurrence include completeness of primary aneurysm treatment. The probability of aneurysm recurrence after complete clip closure within 10 years has been reported to be 0.7%, whereas the risk of recurrence for aneurysms with a retained remnant is 13.9% [20]. Among the risk factors for recurrence, the authors of the aforementioned study from South Korea identified both leftover aneurysms and increased alcohol consumption. Other risk factors for recurrence described include young age of the patient or the presence of multiple aneurysms.

Approximately 6 years after complete treatment with the 699 aneurysm clip, only one aneurysm recurrence (0.14%) was diagnosed [21]. On the other hand, in 59 aneurysms with residual aneurysm on early angiographic examination, eight (13.6%) were found to have grown in the long term. All these eight aneurysms required treatment. A further eight (0.97%) new aneurysms were then diagnosed in this cohort of patients. The results naturally correlate with the issue of endovascularly treated IA, but where recurrence rates are much higher [22]. All of these patients had a primary diagnosis of multiple aneurysms. Several conclusions can be drawn from this. First, that we should always try to treat aneurysms completely. Furthermore, we should perform early angiographic (CTA, DSA) follow-up and treat this if there is a resolvable residual. As far as long-term follow-up is concerned, this should be particularly emphasized in patients with primary incompletely treated aneurysms, in young individuals and also in patients with primary diagnosed multiple aneurysms.

Perhaps for interest it is worth recalling the now obsolete problem related to the recurrence of clipped aneurysms, which appeared at the end of the 1970s. At that time, several case reports were published concerning stress-induced corrosion of some types of aneurysmal clips [23]. Regarding the materials used for clip production, it originally started with silver clips, as silver was considered inert [24]. However, silver clips tended to corrode over time and their use led to a significant reaction of the surrounding tissue. In the next period, stainless steel alloy clips were produced (the first Drake and Yasargil clips). The development of MR in medicine, and especially in neurosurgery, subsequently led to the need for MR-compatible clips. Thus, clips made of special alloys were developed, e.g. MP 35 N (Sundt clips), or cobalt alloys Phynox (Yasargil clips) or Eligiloy (Sugita Standard). However, even these clips do not allow postoperative MR monitoring as they are a source of significant artefacts. Therefore, efforts have been made to develop artifact-free clips, such as ceramic or fiber-reinforced plastic clips [25,26]. The Detroit team of authors found that previously used Heifetz, Pivot, and Vari-Angle clips were more prone to failure than others (e.g., the well-known Yasargil clips). The temporary Yasargil and Sugita clips have closing pressures between 0.88 and 1.08 N (90-110 g) and 0.69 N (70 g), respectively. Permanent clips have a closing pressure of 1.27-1.47 N (130-150 g, Sugita) and 1.47-1.96 N (150-180 g, Yasargil). The closing pressure is not uniform along the length of the gates, but is lowest at the tip and strongest in the proximal part of the gates.

 

Classification of aneurysmal sac recurrence after clipping

Recurrence of an aneurysm is defined as de novo growth of the sac after complete treatment of the aneurysm or enlargement of the residual sac after incomplete treatment. There are several classifications of residual or recurrent aneurysms after clip IA. The first classification was according to Drake in 1967, who divided aneurysms into three grades: 1. complete obliteration; 2. a small portion of the sac is left; 3. a large portion of the sac or the entire sac is left [27]. Probably the most well-known classification is that of Sindou, who divided aneurysm remnants into five grades: 1. less than 50% of the aneurysm neck left; 2. neck of the aneurysm left; 3. part of the sac (lobulus) left in multilobulated aneurysms; 4. part of the sac left, less than 75%; 5. more than 75% of the sac of the aneurysm left [28]. Meanwhile, the authors recommend leaving the first two groups for follow-up, while types 3-5 are primarily indicated for revision.

Another classification from Japan takes the issue of surgical management of recurrent aneurysms one step further [29]. Kobayashi et al. defined the relationship between the existing plane of sac occlusion given by the branching of the original clip and a new plane defined by the optimal position of the branching of the new clip. Thus, this classification helps with the indication of subsequent surgical management of aneurysm recurrence. The authors divide the recurrences into four types with a suggestion of surgical management, where for types I, II and IIIb the authors suggest deployment of a new aneurysm clip followed by removal of the original clip. For type IIIa, the authors then recommend removal of the original clip first to allow deployment of a new clip and complete resolution of the recurrence. For type IV recurrence, where the relationship of the sac to the parent vessels is complex, the authors then suggest surgical treatment in the form of trapping and bypass, as a direct clip does not allow resolution of the recurrence due to the complexity of the sac. In doing so, the authors primarily consider endovascular management of recurrence in all patients. However, given that most IA recurrences do not have a narrow neck and are rather complex, the authors state that endovascular management can be used in a minority of clip-resolved IA recurrences. We have similar experience with this at our institution.

There are two other classifications of IA according to Spiotte and el-Beltagy, which divide relapses similarly according to the relationship of the original clip to the relapse into three categories. The el-Beltaga variant is a very simplified version of the Kobayashi classification, addressing the possibility of deploying a new clip without conflict with the original clip; the Spiotta classification does not directly address the relationship between surgical treatment and type of recurrence. Spiotta et al. described three types of IA recurrence. In type I, recurrence is in the proximal part of the clip, type II in the distal part of the clip, and type III lateral to the branching of the clip [30].

Endovascular treatment for recurrence of IA after clipping

Due to the relatively small number of cases, there are no large randomized trials evaluating the effectiveness of endovascular or surgical treatment in patients with recurrence of surgically treated IA. A Brazilian retrospective observational multicenter study in 70 patients with clip-treated aneurysm or recurrence of aneurysm after clipping who were endovascularly treated has been published [31]. The study showed that immediate complete obliteration of the aneurysm was observed in 73.1% of aneurysms (excluding flow-diverter-treated aneurysms). Complete occlusion after 1 year was observed in 75.3%, but only 68.4% of aneurysms treated with simple coiling, for example. Thus, it is clear that even if endovascular treatment avoids manipulation of the scarred area, the results of treatment are not entirely satisfactory in terms of technical success. The decision to manage the recurrence of a surgically treated hernia is always made as a team with the interventional radiologist, considering both management options (Figure 4).

Dispensarization of patients after surgical treatment of IA

The follow-up of these patients is based on clinical examination and repeated radiological checks, as in the case of endovascular treatment. As far as radiodiagnosis is concerned, the gold standard is evaluation by DSA, optimally 3D DSA. The disadvantage is the invasiveness with the need for femoral artery cannulation, i.e. hospitalization. The risks associated with the procedure itself are relatively small, such as approximately 0.4% risk of hematoma at the injection site or approximately 0.3% risk of temporary neurological deficit [32]. However, due to its invasiveness, this method is unsuitable for regular follow-up. Non-invasive and completely free of X-rays is MRA, however, clip artifacts do not allow evaluation of the area around the clip. Thus, at present, we predominantly follow patients with CTA, which allows, with some limitations, the evaluation of significant residual or recurrent sac aneurysms while allowing outpatient follow-up. The disadvantage, however, is the X-rays. On the other hand, a new ultra-short echo time 3T MR sequence (GE Healthcare Life Sciences, Altrincham, UK) has recently been introduced, which eliminates the influence of metal artefacts on the image and allows relatively accurate assessment of the treated sac and surrounding vessels, offering a promising option in the near future [33]. It can be expected that the further development and extension of this and similar sequences will likely lead to patients being radiologically monitored with MR after aneurysm clipping, thereby avoiding radiation exposure. On the other hand, before actually deciding and planning treatment of the aneurysm recurrence, we prefer high-quality 3D CTA and, if it is not available, we recommend performing 3D DSA, which, for example, is nowadays rarely used for primary aneurysms.

The question is how long or whether to follow patients for life after aneurysm clip treatment [9,18,34-36]. A recent meta-analysis has shown that the recurrence rate after clip treatment as well as de novo aneurysms increases more or less linearly over time [35]. The results of the aforementioned meta-analysis also confirm the need for long-term follow-up, with the authors recommending follow-up dates at 5, 10 and 20 years after treatment. A second benefit may be the detection of unruptured aneurysm, which the authors of the above meta-analysis report to be around 7% after 20 years. We therefore agree with active and long-term/life-long follow-up of patients after treatment of cerebral aneurysm [35,37].

 

Conclusion and recommendations

Surgical treatment of IA is more stable in the long term compared to endovascular treatment. On the other hand, the risk of residual or recurrence even in the best hands is 7% over 10 years. The risk of recurrence including bleeding is higher in incompletely treated aneurysms. Therefore, during primary treatment, efforts should be made to completely resolve the bulge if it is safe to do so. Completeness of IA treatment should be verified by CTA or DSA early after surgery. Long-term follow-up of all treated patients is also necessary as the risk of recurrence increases over time. This should be particularly emphasized in aneurysms with retained remnant. In patients with recurrence, it is not possible to say which type of treatment (either endovascular or surgical) is better, and this must be considered on a completely individual basis, based on the anatomical conditions, the patient's age, their condition, etc. A detailed radiological diagnosis is necessary before such a decision, optimally by 3D DSA if there is any uncertainty after CTA. Surgical treatment then requires careful preparation of the aneurysm and parent arteries in the scarred area and readiness for the necessity of improvisation in the surgical treatment of the aneurysm, as postoperative changes and the already deployed clip often do not allow a simple, straightforward solution.

 

Financial support

The work was supported by the internal grant of Krajská zdravotní, a. s., IGA-KZ-2020-1-15, IGA-KZ-2023-1-13 and the grant of the Agency of Medical Research of the Ministry of Health NU22-08-00124.

 

Conflict of interest

The authors declare that they have no conflict of interest in relation to the subject of the paper.