Key-words:
Aneurysms - endovascular coiling - management - recurrence
Introduction
Clipping and endovascular coiling (EC) are both viable modalities of management in
intracranial aneurysms. The modern world has witnessed a recent surge in advancements
of EC. The balance between the two has been shifted more in favor of EC in the recent
times, especially in the developed countries. The complete obliteration rates of intracranial
aneurysms in the EC group has been showed to be inferior to the clipping group in
the previous studies.[[1]] The International Subarachnoid Aneurysm Trial reported that 26% of angiograms showed
neck remnants and 8% showed refilling after coiling compared with 12% and 6%, respectively,
in the clipping group.[[2]],[[3]] The Cerebral Aneurysm Rerupture After Treatment study revealed annual retreatment
rates of coiled and clipped aneurysms of 13.3% and 2.6%, respectively, during the
1st year after intervention.[[4]] The study also emphasized that rupture after residual aneurysms were directly related
to the degree of neck occlusion. The annual risk of rupture for completely occluded
aneurysms were 1.1%, whereas it was 5.9% for aneurysms neck occlusion of 70%–90%.
These residual aneurysms have potency to regrowth and subsequent rerupture. As a sequalae
to the upsurge of EC in the developed world, there has been an increase in the incidence
of recurrent aneurysms (RAs). These RAs pose a unique challenge to the treating surgeons
as opposed to the primary aneurysms because of the unfavorable configuration imparted
by the initial coiling. In this retrospective study from our institution, we discuss
the demography of patients, angiographic patterns, treatment strategies, and the outcome
of RA.
Materials and Methods
A retrospective analysis of case records of the Bantane hospital, Fujita Health University,
from the period 2014 to 2019 was done. Patients' demography and aneurysm characteristics
were noted. The patient demographics included age, sex, and comorbidities. Whereas,
the aneurysm characteristics studied were location of aneurysm, size at the time of
clipping, number of endovascular procedures before clipping, surgical indications,
techniques, and outcome of the procedure.
Outcome
The outcome was dichotomized into good and bad outcome depending on the Glasgow Outcome
Scale (GOS). Good outcome was classified according to GOS 4 and 5, whereas bad outcome
was classified in patients with GOS 1, 2, and 3. Any complications occurring during
the follow-up time was recorded and graded into minor and major complication. Minor
complications were defined as any temporary neurologic deficit not needing intervention,
any cranial nerve palsy, and wound infections. Major complications included any intervention
in the form of surgery or placements of any shunt and any complication, resulting
in permanent disabling neurological deficit or death.
Statistical analysis
All recorded continuous variables will be expressed as means and qualitative variables
will be expressed as proportions.
Results
There were three cases of RAs after EC in our institution in the above-mentioned period.
One patient with giant vertebral aneurysm who underwent stent-assisted coiling outside
of our institution, presented to us with hemiparesis due to mass effect on the brainstem
and hence was reoperated here. There were three males and one female. The mean age
of the patients was 52.2 ± 3.4 years. The mean size of the RAs was 17 ± 5.1 mm, which
included two giant aneurysms as well. Two patients underwent coiling more than once.
Among them, one patient had stent-assisted coiling for a giant vertebral artery aneurysm.
The time to recurrence between coiling and final clipping was between 2 and 3 years.
All patients underwent direct clipping of aneurysm. In three patients, the aneurysm
was amenable to direct clipping without manipulation of the coils, whereas in one
patient, it was necessary to remove the coils from within the aneurysm to facilitate
clipping. This patient had a giant vertebral artery aneurysm, for which he underwent
proximal and distal trapping along with the occipital artery to posterior inferior
cerebellar artery bypass. Summary of data has been described in [[Table 1]].
Table 1: Patient demographics, aneurysm characteristics, and outcome
Illustrative cases
Case no 1
A 58-year-old male was detected to have a distal anterior cerebral artery (DACA) aneurysm
in 2008, for which he had underwent coiling. After 1 year, recurrence of the aneurysm
was noted and he again underwent coiling in 2009. In 2015, on routine follow-up angiography,
there was Raymond–Roy occlusion classification (RROC) Gr2 recurrence [[Figure 1]]a. There was coil compaction on angiography. He underwent bifrontal craniotomy and
interhemispheric approach for the clipping of aneurysm. Intraoperatively, the coils
were extruding out of the aneurysmal sac [[Figure 1]]b. No coil extraction was attempted. The neck was well defined due to coil compaction.
The aneurysm was clipped effectively. The digital subtraction angiography (DSA) and
intraoperative photograph are depicted in [[Figure 1]].
Figure 1: (a) Digital subtraction angiography showing filling of the neck of the aneurysm sac
with contrast due to coil compaction. (b) Intraoperative photograph of the coiled
aneurysm. Note the coils are seen embedded in the wall of the aneurysm. Some parts
of the coil are seen to be extruded from the sac
Case no 2
A 44-year-old female underwent coiling for the right internal carotid artery posterior
communicating artery aneurysm in 2015. On follow-up angiogram after 2 years, she had
RROC Gr 2 recurrence of the aneurysm [[Figure 2]]a. She underwent right pterional craniotomy and trans-Sylvian approach for the clipping
of aneurysm in 2017. Intraoperatively, the coils were seen embedded in the wall of
the aneurysmal sac and no attempts were made to remove them [[Figure 2]]b. The aneurysm was clipped without any residual neck. The DSA and the intraoperative
photograph are depicted in [[Figure 2]].
Figure 2: (a) Digital subtraction angiography of the patient showing aneurysm in the communicating
segment of the internal carotid artery. Note the neck is well visualized with filling
of the contrast. (b) Intraoperative photograph showing the aneurysm with coils embedded
in the aneurysm sac (short arrows). There is no extrusion of coils
Case no 3
A 50-year-old male was detected to have a partially thrombosed giant Vertebral artery
aneurysm in 2014 [[Figure 3]]a. He underwent coiling of the aneurysm in the same year. In the follow-up angiogram
a year later, it was observed that there was a recurrence of aneurysm and he again
underwent stenting and coiling in 2015. In the subsequent year, there was rerecurrence
and he underwent coiling in 2016 [[Figure 3]]a. In 2017, the patient presented with progressive diplopia, left facial weakness
along with dysarthria and dizziness. He was investigated with angiogram during which
it was detected that the aneurysm showed progressive growth [[Figure 3]]b and [[Figure 3]]c. There was evidence of mass effect on the brain stem on magnetic resonance imaging.
It was decided that the patient be managed with surgery and relieve the mass effect
of the growing aneurysm on the brain stem. He underwent suboccipital craniotomy during
which the aneurysm was seen in close proximity to the lower cranial nerves and the
Pica was seen running along the stalk of the aneurysm from the vertebral artery [[Figure 3]]d and [[Figure 3]]e. The aneurysm was managed with proximal and distal trapping with aneurysm clips.
The aneurysm was opened and the coils were retrieved from within the aneurysm sac
[[Figure 3]]f and [[Figure 3]]g. The stent was left intact within the aneurysm. The excision of the redundant
sac was done. This was followed by the occipital artery to posterior inferior cerebellar
artery bypass. Postoperatively, the patient did well. The dysarthria had resolved,
but the facial nerve palsy recovered only partially.
Figure 3: (a) Magnetic resonance imaging brain T2-weighted axial image showing giant thrombosed
aneurysm with mass effect on the brain stem. (b) Follow-up imaging with the same sequence
after 3 years showing growth of the aneurysm with increased mass effect on the brain
stem. (c) Digital subtraction angiography depicting the large vertebral artery aneurysm.
(d) Intraoperative view of the aneurysm An - Aneurysm; LCN - Lower cranial nerves.
The encircled area demonstrating stalk between the vertebral artery and the aneurysm.
(e) The intraoperative field being inspected by an endoscope. VA - Vertebral artery,
An - Aneurysm, PICA - Posterior inferior cerebellar artery. (f) The aneurysm being
opened intraoperatively. (g) The coils within the aneurysmal sac (black arrows) being
removed intraoperatively
Case no 4
A 60-year-old male had undergone treatment with coiling in 2017 for a subarachnoid
hemorrhage due to aneurysm rupture. The aneurysm was located at the DACA. In the following
year, he underwent coiling for the same aneurysm twice in interval of 7 months as
the aneurysm showed recurrence during follow-up angiogram. After 6 months, a follow-up
angiogram was done, and it was noted that the aneurysm showed RROC gr3 recurrence
[[Figure 4]]a. At this juncture, it was decided to treat the aneurysm surgically. In a view
to maintain the distal supply to the anterior cerebral artery ipsilateral to the aneurysm,
a salvage bypass was initially done with a midline frontal craniotomy whereby a superficial
temporal artery graft to A3 was done. This was followed by a pterional craniotomy
and the aneurysm clip was applied distal to its origin of the aneurysm on the non-dominant
A1. Operative plan is illustrated in [[Figure 4]]b. This was done to dampen the flow into the aneurysm sac and induce thrombosis
as well as to maintain flow to the perforators of the aneurysm from dominant A1 on
the opposite side through the anterior communicating artery. The DACA distal to the
aneurysm was perfused by interposition of a superficial temporal artery graft.
Figure 4: (a) Reconstructed computed tomography angiogram showing left A1 giant aneurysm (green
color). (b) Illustrative diagram of the operative plan. The aneurysm was clipped at
the A1-A2 junction distal to the aneurysm. The superficial temporal artery was anastomosed
to the A3 part of the anterior cerebral artery
Discussion
EC of aneurysms, though minimally invasive in nature, is not without complications.
Literature has shown that approximately 20% of coiled aneurysms are associated with
recurrence, of which 10% will undergo additional intervention.[[5]],[[6]] A synopsis of cases available in the literature regarding surgery for recurrent
aneurysms followins coiling and outcome in the last five years is summarised in [[Table 2]]. Ogilvy et al., analyzed the risk for recanalization of aneurysms and noted that
size more than 10 mm, neck size >4 mm, rupture, stent assistance, and posttreatment
degree of aneurysm occlusion were significant factors for recanalization of aneurysms
following endovascular treatment.[[7]] In the recently published results of 10 years of the BRAT showed that rates of
aneurysm obliteration decrease and the rates of retreatment increase over the time
in patients who underwent EC.[[8]]
Table 2: A synopsis of major series published cases in the English literature in the last
5 years
The indications for surgery in patients after EC are: (a) presence of remnants after
coiling, (b) recanalization and regrowth of previously coiled aneurysms, (c) mass
effect of the coiled aneurysms, and finally (d) migration of the coils.[[9]] In our experience, we had three patients, in whom there was a recanalization of
the aneurysm, whereas, in one (Case no 3), there was true growth of the aneurysm.
In this patient, the growing aneurysm was pressing itself against the brain stem.
Hence, it was prudent to relieve him of the mass effect on the brain stem.
The recanalization of aneurysms after EC has been classified by various authors. Grunwald
et al. classified the recanalization patterns into ones with coil mesh change (Type
a), neck growth (Type b), and dog ears (Type C1 and C2).[[10]] Widely accepted classification scheme for recanalization after EC was published
by Raymond et al.[[11]] and mentioned as Raymond-Roy occlusion Classification (RROC). They classified recanalization
depending on the angiographic pattern of contrast enhancement into three, viz, total
occlusion (RROC1), contrast filling the neck (RROC2), and any contrast into to the
aneurysm dome (RROC3). Mascitelli et al. further subclassified RROC3 into: (a) any
contrast into the interstices of the coils within the aneurysm and (b) contrast enhancement
into the wall of aneurysm.[[12]] This was done in view of subanalysis which showed the risk of recanalization and
rerupture to be highest in Group 3B. Kobayashi et al. described RAs according to the
plane of closure of the clip and the plane of neck of the aneurysm into four types
and derived a plan of algorithm for each type.[[13]] The reasons for treating RAs can be due to either coil compaction or true aneurysm
regrowth. In this scenario, a second EC is an option in the management with most of
the recurrences. With the advances in the endovascular technique, many recurrent aneurysms
have been managed effectively with stenting/stent-assisted [[14]],[[15]],[[16]] coiling as well as pipeline embolization [[17]] devices, but this expertise may not be available in all centers and not all aneurysms
are suitable for this type of intervention by virtue of its unfavorable anatomical
configuration, namely, wider neck and mass effect. Moreover, stent-assisted coiling
has been shown to be associated with more complications [[18]] as well as recurrences [[19]],[[20]] in view of the dual antiplatelets therapy required for long-term patency.[[21]] Hence, many centers opt for clipping in this scenario.
Aneurysm characteristics that favor effective clipping following endovascular coiling
The difficult part after exposing the RA is to clip it in a configuration that would
best maintain the patency of the parent vessel as well as the perforators arising
from it. Many times, the surgeon may not be able to position the clips where he intends
to as the clip blades may slip into the parent artery due to the mass occupied by
the coils within the aneurysm. These factors should be kept in mind and the best possible
clip and the plan of clipping which can cater to the given situation should be chosen.
Many authors have described the favorable characteristics for clipping following recurrences
after EC. Toyota et al. stated that RA type 3 (tall remnant neck) and RA type 4 (short
remnant neck but distinct demarcation between thrombosed and nonthrombosed part) are
the most favored type for selective clipping.[[22]] Alternatively, Waldron et al. noted that the ratio of coil width to compaction
height was a reliable indicator of clippability. The coil width to height ratio <2.5
are good candidates for clipping, whereas others require additional technical options
like bypass.[[23]] Kobayashi et al. described in their experience that RAs after EC can be safely
clipped without the old clip interfering with the new one in Type 1, 2, and 3b, whereas
Type 3a and 4 require more complex procedures such as bypass or endovascular treatments.[[13]]
Surgical techniques and challenges
The primary challenge in the management of RAs is to dissect the aneurysm in the field
of fibrosis induced by the partially or totally extruded coils placed during the endovascular
intervention. The accurate placement of clips during surgery is difficult and often
involves removal of the coils placed during EC to define the neck. This process has
been found to be an adverse factor in the outcome of clipping after EC. The ideal
aneurysm characteristics for clipping after coiling are those with narrow neck and
coils not protruding in the parent vessel. Removal of coils from the recanalized aneurysm
offers a technical challenge as coils become incorporated into the aneurysm wall as
early as 2 weeks after placement, and their removal therefore becomes riskier over
time.[[24]],[[25]] In our limited experience, we had only one patient, in whom it was necessary to
remove the coils. In this patient (Case no 3), this procedure was inevitable in the
process of excision of the growing aneurysm to relieve the mass effect on the brain
stem. In view of complex anatomical recurrences, it is essential to have a complex
surgical procedure in the form of cerebrovascular bypass. This can be achieved by
a in situ bypass selecting an appropriate neighboring artery or by inserting an interposition
graft. A meticulous surgical plan must be delineated before the commencement of the
surgery in such complex configuration of RAs.
Limitations
The case series is limited by small sample size, hence no accurate derivations can
be drawn. Larger sample size is required to draw accurate management algorithms in
cases of RAs following EC.
Conclusion
RAs possess a complicated dilemma in outlining an optimal management plan. These aneurysms
have to be dealt with surgeons and large volume centers that handle complicated neurovascular
surgery, including complicated cerebrovascular bypasses. The best method of treatment
should be discussed in a multidisciplinary team consisting of both endovascular as
well as open surgery, with the aim of providing sustainable result with minimal morbidity[[33]].
Declaration of patient consent
The authors certify that they have obtained all appropriate patient consent forms.
In the form the patient(s) has/have given his/her/their consent for his/her/their
images and other clinical information to be reported in the journal. The patients
understand that their names and initials will not be published and due efforts will
be made to conceal their identity, but anonymity cannot be guaranteed.
