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Interv Neuroradiol. 2016 August; 22(4): 413–419.
Published online 2016 May 12. doi:  10.1177/1591019916647193
PMCID: PMC4984392

Intracranial post-embolization residual or recurrent aneurysms: Current management using surgical clipping

Abstract

Post-embolization residual or recurrent aneurysms (PERRAs) are not rare in patients with intracranial aneurysms treated by embolization. Their occurrence is mainly associated with an increased amount of interventional therapy. Repeated interventional embolization can be applied in some patients with PERRAs, whereas surgical clipping is preferred in other cases that are not suitable for repeated interventional embolization due to the difficulties inherent to this operation. The surgical clipping of PERRAs is very complicated and difficult to perform, and relevant reports are rare. This study offers a review of PERRA treatment using surgical clipping. Retrospective studies have shown that PERRAs are common aneurysms of the anterior and posterior communicating arteries. According to the recurrent characteristics of PERRAs, it is reasonable to categorize PERRAs into three types: type I—coils are compressed, and no embolic material fills the neck of the aneurysm; type II—coils are migrated, and very few coils fill the neck of the aneurysm or the parent artery; and type III—coils are migrated, and multiple coils fill the neck of the aneurysm or the parent artery. Direct clipping can be applied to types I and II PERRAs, whereas trapping, wrapping, or auxiliary revascularization is required in type III PERRAs. Most coils do not require removal unless they interfere with clipping. However, it is necessary to avoid damaging the surrounding adhesive tissue during coil removal. Satisfactory therapeutic outcomes can be achieved by selecting appropriate PERRA cases in which to perform surgical clipping.

Keywords: Embolization, residual and recurrent aneurysms, clipping, prognosis

Introduction

Intracranial aneurysm embolization is an effective approach to the treatment of aneurysms, and features reduced trauma and fast recovery.1,2 Currently, more physicians are opting to use this approach as a first-line treatment strategy. The results of the Barrow Ruptured Aneurysm Trial (BRAT), the International Subarachnoid Aneurysm Trial (ISAT), and another randomized trial of endovascular versus surgical treatment of ruptured cerebral aneurysms from Finland suggest little difference in outcome between the endovascular coiling and neurosurgical clipping treatments for anterior circulation aneurysms; for posterior circulation aneurysms, coil embolization appears to provide a sustained advantage over clipping. However, aneurysm obliteration rates are significantly lower and retreatment rates significantly higher in patients undergoing coiling than in those undergoing clipping.35 Consequently, the most serious drawback of cerebral aneurysm coiling is its high recurrence rate, which necessitates additional retreatment to reduce the risk of future hemorrhage.6,7 Reportedly, approximately one-fifth of all coiled cerebral aneurysms recur, and 10% of coiled aneurysms require additional intervention.8

Repeated interventional embolization can be applied to cases with post-embolization residual or recurrent aneurysms (PERRAs). In 2013, Tahtinen reported that 55 patients with 56 PERRAs were electively retreated using stent-assisted embolization, and satisfactory outcomes were achieved.9

In addition, the introduction of flow diversion in recent years has promoted another effective treatment for PERRAs.10 In 2015, Daou et al. treated 33 cases of PERRAs with a pipeline embolization device and concluded that use of the flow diverter to manage PERRAs is safe and effective for aneurysm occlusion.11

However, problems (in particular, a higher recurrence rate) have emerged in interventional endovascular embolization therapy for PERRAs.11,12 Some patients have even experienced repeated relapse of PERRA. For instance, Kang et al. in 2006 reported a group of patients with PERRAs, some of whom experienced multiple repeated recurrences.13 In some PERRA cases, it was difficult to create a stable basket in the recanalized aneurysms because the recanalized portions were also small and the introduced coil did not form a mesh with the previous coil mass.14 In such cases, endovascular coiling is not feasible and does not produce stable occlusion of the aneurysm. Thus, the surgical treatment of previously coiled aneurysms is necessary in some patients.2,15

Because the best neurosurgical strategy and technique for PERRA treatment remains a subject of debate and because recent relevant reports are rare, it is difficult to have an overall sense of the best method of treating previously coiled aneurysms. Hence, the aim of this study was to review the current management of PERRAs using surgical clipping and to document its progress.

History of surgical clipping for PERRAs in recent years

As early as 1995, Gurian et al. categorized these factors into three groups: group A, failed embolization; group B, residual and recurrent aneurysms; and group C, postembolization complications.16 In 2007, Tirakotai et al. classified the indications for surgical treatment after the coiling of aneurysms into the following three groups: (1) surgery of residual and recurrent aneurysms; (2) surgery for mass effects on neural structures due to coil compaction; and (3) surgery for vascular complications after endovascular procedures.17 Group B in Gurian’s study and the first group of Tirakotai’s study were particularly noteworthy and intractable because intra-aneurysmal coil masses are sometimes scarred to the aneurysm wall or adherent to adjacent vital structures. Other studies have produced similar results, and the literature not listed in this section is presented in Table 1.1821 In recent years, the treatment of PERRAs has never ceased; an increasing number of studies have been performed to treat PERRAs. With the growing volume of aneurysms treated using endovascular methods and the unavoidable risks of incomplete coiling or recurrence, the volume of PERRAs requiring surgical management is increasing accordingly.22 Therefore, it is necessary to review the current state of PERRA treatments.

Table 1.
Reviewed literature not listed in the paper.

Clinical features of PERRAs

PERRAs show certain clinical characteristics. They typically manifest as subarachnoid hemorrhages (SAHs), with a tendency to occur as aneurysms of the anterior communicating and posterior communicating arteries. In 2011, Romani et al. retrospectively analyzed 82 PERRAs in 81 patients who underwent surgical clipping. Of the 81 patients in this study, 53 (65%) were women; the median time between coiling and surgery was 12 months (range 0–84 months). SAH was present in 61 (74%) of the cases; 14 (17%) were incidental, and a mass effect was present in seven (9%). Thus, hemorrhage was the highest factor predisposing to PERRAs. In the anterior circulation, PERRAs were, most commonly, aneurysms of the anterior communicating artery; next most commonly, aneurysms of the middle cerebral artery; and least commonly, aneurysms of the posterior communicating artery. In the posterior circulation, the basilar bifurcation was the most common site.23 In 2015, Owen et al. reported 73 cases of PERRA, of which 58 were women. Overall, 64 (88%) patients presented with SAH; the remainder presented with mass effect symptoms from giant aneurysms, headache, or incidental aneurysms. Among 56 cases of anterior circulation aneurysms, PERRAs were most commonly anterior communicating artery aneurysms, followed by posterior communicating artery aneurysms and middle cerebral aneurysms. Of the 17 cases of posterior circulation aneurysms, PERRAs most commonly occurred as basilar bifurcation aneurysms, followed by posterior inferior cerebellar artery aneurysms.21 Other studies have produced similar results. The literature not listed in this section is presented in Table 1.19,20,2426

It is obvious that the data from different sources are not consistent. However, SAH is present in the majority of PERRA cases, and anterior and posterior communicating artery aneurysms are the most common sites of PERRA occurrence.

Classification of PERRAs and strategies for their treatment

Neurosurgical clipping is an effective method for treating ruptured PERRAs. When coil embolization is used to treat ruptured aneurysms, stent-assisted coiling is usually required, and this procedure must be followed by postoperative dual antiplatelet therapy. Dual antiplatelet therapy is one of the most important risk factors for surgical complications.27 However, it can be avoided if PERRAs are treated by neurosurgical clipping, which is relatively safe and ensures aneurysm closure.3 In 2003, Deinsberger et al. reported seven cases of ruptured PERRAs. Good clinical outcomes were achieved in all of these patients after neurosurgical clipping. This study indicates that the achievement of good results is possible, although technical challenges are frequently encountered. However, the treatment must be carefully planned, and the surgical approach is determined by the need for coil removal and the amount of time that has elapsed since coiling.28

Surgical management of PERRAs by surgical clipping mainly depends on the type of PERRA. In the literature, PERRA types have been categorized as follows: type I coils are compressed, and no embolic material fills the neck of the aneurysm; type II coils are migrated, and very few coils fill the neck of the aneurysm or the parent artery; and type III coils are migrated, and multiple coils fill the neck of the aneurysm or the parent artery (Figure 1). Direct clipping can be used in type I and II PERRAs, although the procedure may be challenging. Type III PERRAs are difficult to treat, and clipping cannot be used in this type. Revascularization is required after the aneurysm is trapped, or wrapping only can be performed. During surgery for PERRA treatment, a decision must be made whether to open the aneurysm and remove the coils. When the coils interfere with neck clipping or are mainly located in the aneurysmal body and dome, they can be removed, thereby reducing tension and compression of the surrounding tissue. When the coils are located in the neck of the aneurysm or even in the parent artery or when they have migrated into the surrounding normal tissue and are difficult to remove, it is not necessary to force the removal of coils.

Figure 1.
Classification of post-embolization residual or recurrent aneurysms. (a) type I—coils are compressed, and no embolic material fills the neck of the aneurysm; (b) type II—coils are migrated, and very few coils fill the neck of the aneurysm ...

In 2007, Raftopoulos et al. summarized 17 cases of PERRAs and classified specific treatment methods for three groups of type I and II PERRAs: group A cases, characterized by an aneurysm residue that allows direct surgical clipping as assessed preoperatively; group B aneurysms, with a residue smaller than predicted and showing parent vessel stenosis where the clip was applied to the neck remnant (these require the fundus full of coils to be removed followed either by clip application to the neck residue or by suture if the remnant is too small); and group C cases, requiring coil extraction through the parent vessel or through the fundus.29 This grouping may serve as a guideline for the surgical management of PERRAs using surgical clipping.

Current management of PERRAs using surgical clipping

Current experience in the management of PERRAs has been obtained from multiple-case studies. Gurian’s 1995 study included 196 cases with embolization therapy and found 10 cases of PERRAs during follow-up; surgical treatment was utilized in these cases. Of these, seven were considered type I or II PERRAs, for which one or more aneurysm clips were used to occlude the aneurysms; three cases were considered type III PERRAs, for which aneurysm trapping and bypass were used. However, the coils were not removed in the majority of the cases.16 These studies show that surgical treatment is relatively simple in the case of type I or II PERRAs but complicated in type III PERRAs.

Better outcomes can be achieved if the appropriate treatment method is selected for type I or II PERRAs. In 2011, a multiple-case study by Romani et al. described 81 patients with 82 PERRAs that were microsurgically treated. Of these, 78 aneurysms of type I or II PERRAs were directly clipped, two aneurysms of type III PERRAs were trapped, and two aneurysms of type III PERRAs were trapped as well as bypassed.23 In 2014, Rubino et al. reported 20 cases of PERRAs, all of which were type I or II and were directly clipped. This outcome may be attributed to a better understanding of PERRAs and the appropriate selection of patients.30

Therefore, it is reasonable to categorize PERRAs into types I, II, and III as a basis for determining whether surgical clipping can be used for their treatment. However, the choice of treatment method for PERRAs also depends on other factors. In 2006, Minh et al. concluded that, in particular, an aneurysm height-to-neck ratio of less than 2:1 after coiling and the use of stent-assisted coiling presented formidable challenges to direct clipping.31 The difficulty of treatment is especially increased when the aneurysm is large and located within the posterior circulation.

During the clipping procedure for PERRAs, the choice to remove the previous coils depends on the following conditions. Coils should be removed if they interfere with the operation or cause a mass effect. In 2008, Lejeune reported 21 cases of PERRAs; coils were removed in most cases.24 However, Izumo et al. reported seven cases of PERRAs. Microsurgical clipping without coil removal was used in six patients with type I or II PERRAs, and the one case with a type III PERRA was trapped using parent artery occlusion under bypass.26 Thus, a variety of outcomes were observed in different studies, and this was mainly associated with patient selection.

At the time of clipping the aneurysm, whether the previously embolized coils can be successfully removed often depends on the time that has elapsed since embolization. If a relatively long time has elapsed, the coils may extrude from the aneurysm and be covered by the surrounding tissue. Thus, removing them may be very difficult. If the time course is short, the coils can often be easily removed.32 In 2000, Thomton reported 11 cases that underwent surgery following embolization. Most of these patients underwent craniotomy a short time after the embolization procedure. The coils were removed at the time of surgery in nine cases.33 In 2011, Romani et al. performed clipping procedures for 82 PERRAs in 81 patients. Clipping without coil removal was performed in 50 aneurysms (61%), complete coil removal was performed in 21 aneurysms (26%), and the partial removal of coils was performed in seven aneurysms (9%). Complete coil removal was accomplished significantly more often in the early surgery group than in the late surgery group. During surgery, the removal of coils can provide space for clipping the aneurysms, but the forced removal of coils can cause more severe trauma. The best outcome was achieved in the group in which the aneurysm could be clipped without coil removal.23 Other studies have produced similar results. The literature not listed in the section is presented in Table 1.18,19,25,30,34,35

During the PERRA operation, coils should be removed if it is necessary. However, premature manipulation of a recently coiled aneurysm sac, especially if loosely coiled for any reason, can be associated with thromboemboli dislodging from the sac and passing into branch arteries.

Surgical outcomes of PERRAs

Currently, PERRA management using surgical clipping can yield satisfactory outcomes. The studies by Waldron et al. in 2009,19 by Veznedaroglu et al. in 2004,18 and by Thornton et al. in 200033 show consistent and favorable outcomes. In addition, the surgical outcomes of early- and late-stage PERRAs were compared in a 2011 study by Romani et al. This study retrospectively analyzed 81 patients with 82 previously coiled aneurysms that were microsurgically treated at two Finnish neurosurgical university hospitals. Fifty-eight PERRAs located within the anterior circulation and 24 PERRAs located within the posterior circulation were included in this study. Fifteen patients were operated on within the first month (early surgery) after coiling, whereas 66 were treated later (late surgery). Good clinical outcomes were achieved in 71 patients (88%). This study included by far the largest number of cases and may be representative.23

In recent years, the efficacy of therapy for PERRAs has been significantly improved due to a better understanding of PERRAs. In 2015, Petr conducted a meta-analysis of 26 studies involving 466 patients and 471 intracranial aneurysms. The results of this meta-analysis suggest that surgical treatment is safe and effective, and support the idea that aneurysms that are amenable to direct clipping have superior outcomes. Late surgery was also associated with better clinical outcomes. The surgery for recurrent posterior circulation aneurysms was associated with high rates of morbidity and mortality. However, a case-by-case basis considering anatomical factors such as aneurysm location, feasibility of coiling, and local neurosurgical and endovascular expertise should also be considered.36 Other studies have produced similar results. The literature not listed in this section is shown in Table 1.20,21,30 Consequently, the surgical clipping of PERRAs can yield satisfactory results if appropriate patients and approaches are selected.

Summary

Satisfactory therapeutic outcomes can be achieved by selecting appropriate cases of PERRAs for surgical clipping. According to the recurrent characteristics of PERRAs, it is reasonable to categorize PERRAs into types I, II, and III as a basis for determining whether surgical clipping is suitable. Direct clipping can be used with type I and II PERRAs, whereas trapping with/without revascularization or wrapping was preferred in type III PERRAs. In most cases, it was not necessary to remove the coils unless they interfered with clipping. However, if the coils are to be removed, it is critical to avoid damage to the surrounding adhesive tissue.

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

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