Journal of Neuroradiology (2013) 40, 54—61

Available online atwww.sciencedirect.com

CASE REPORT

Delayed rupture of a basilar artery aneurysm treatedwith coils: Case report and review of the literature
Arihito Tsurumi a,∗, Yuko Tsurumi b, Makoto Negoro c, Shinichiro Tsugane a,
Misaki Ryuge d, Noriyuki Susaki a, Toshiki Fukuoka a, Shigeru Miyachi eaDepartment of Neurosurgery, National Hospital Organization Nagoya Medical Center, Nagoya, Japan
Department of Neurosurgery, Japanese Red Cross Nagoya Daiichi Hospital, Nagoya, Japanc
Department of Neurosurgery, Fujita Health University School of Medicine, Toyoake, Japand
Department of Respiratory Medicine, National Hospital Organization Nagoya Medical Center, Nagoya, Japane
Department of Neurosurgery, Nagoya University Graduate School of Medicine, Nagoya, Japanb

KEYWORDS
Aneurysm;
Rupture;Complications;
Embolization;
Intracranial

Summary Delayed rupture of a previously unruptured cerebral aneurysm after uneventful
saccular coil packing is rare, particularly when the quality of aneurysm occlusion is appropriate(neck remnant or total occlusion). The present report describes the case of a 70-year-old woman
with an incidentally detected, asymptomatic, small basilar tip non-thrombosed aneurysm who
experienced rupture of the aneurysm 2 years after coiling. Cerebral angiography taken on the
day of rupture revealed only small recanalization of the aneurysm neck with no dome-ﬁlling. Thisis the ﬁrst report of delayed rupture due to minor recurrence of a previously unruptured small
asymptomatic cerebral aneurysm after saccular coil packing. A literature review of 26 reportsof late bleeding after coil embolization of previously unruptured cerebral aneurysms showedthat dome-ﬁlling after coil embolization, symptomatic aneurysms and large/giant aneurysms
all increase the risk of delayed rupture in previously unruptured aneurysms after saccular coilpacking.
© 2013 Published by Elsevier Masson SAS.

Introduction
The efﬁcacy of endovascular coil embolization in the
management of unruptured cerebral aneurysms has beencharacterized in several large studies [1,2], and delayed∗ Corresponding author. 4-1-1 San-nomaru, Nakaku, Nagoya, 4600001, Japan. Tel.: +81 52 951 1111; fax: +81 52 951 0664.
E-mail address: tsurumi@med.nagoya-u.ac.jp (A. Tsurumi).

rupture of a previously unruptured cerebral aneurysm after
uneventful saccular coil packing is a rare event [3,4].

Case report
A 70-year-old woman was incidentally diagnosed with anasymptomatic basilar tip aneurysm on magnetic resonanceimaging (Fig. 1) and magnetic resonance angiography (MRA).
Her history was notable for hypertension, hyperlipidemia
and coronary artery disease (treated with aspirin 100 mg
daily), but she had no history of subarachnoid hemorrhage.

0150-9861/$ – see front matter © 2013 Published by Elsevier Masson SAS.
http://dx.doi.org/10.1016/j.neurad.2012.08.005

Delayed rupture of saccular coil-packed aneurysm

55

Figure 1 Brain MRI (T1- and T2-weighted images) taken prior to initial embolization. The basilar tip aneurysm is seen with no
thrombus or perianeurysmal edema.

Transarterial coil embolization of this unruptured basilar
tip aneurysm (diameter: 7.4 mm; Fig. 2 A—D) was performed, and 95% neck-remnant occlusion of the aneurysm
was achieved using a balloon-neck remodeling technique(Fig. 2E). Computed tomography performed the next day
showed no subarachnoid hemorrhage (Fig. 3).
MRA at 6 months after the ﬁrst intervention revealed
complete obliteration of the aneurysm (Fig. 4). However,after 18 months, MRA showed small recanalization at theneck of the aneurysm (Fig. 5).
Then, at 22 months after the initial treatment, thepatient presented with subarachnoid hemorrhage (Hunt andHess grade 3, Fisher group 3; Fig. 6A). Cerebral angiography demonstrated a small recurrence at the level of theneck of the basilar tip aneurysm with no other intracranial
aneurysm (Fig. 6B—D). On the day of onset, transarterial coilembolization was performed, using a balloon-neck remodeling technique. During the chronic phase of subarachnoid
hemorrhage, endovascular treatment was performed with astent-assisted coil embolization technique, deploying twoenterprise stents (Cordis Neurovascular, Miami Lakes, FL,USA) in a Y conﬁguration and inserting coils through thestent mesh (Fig. 6E). Triple antiplatelet therapy, comprising aspirin 100 mg daily, cilostazol 200 mg daily and ozagrel
160 mg daily, was maintained during the perioperative
period of stent-assisted coiling. The patient experienced
neurological recovery up to a modiﬁed Rankin Scale scoreof 1.

Discussion
Delayed rupture after saccular coiling
In the published literature, there are 26 reports of late
bleeding after coil embolization of previously unruptured
aneurysms (Table 1) [5—21]. Ten were symptomatic andonly one was asymptomatic at the time of initial presentation. In the other 15 cases, the presence or absence ofsymptoms was not reported. However, two of these 15 cases

Cases reported in the published literature of delayed rupture of previously unruptured cerebral aneurysms after coil embolization.

Authors, year

Aneurysm location

Size

Results ofembolizationa

Occlusion rate attime of rupture

Embolization to
rupture time lag

Guglielmi et al., 1992 [5]Basilar tip

Giant

Residual aneurysm—

18 months

ApSimon et al., 1995 [6]Basilar tip

Large

Residual aneurysm

Residual aneurysm

7 months

Partially thrombosed aneurysm

Malisch et al., 1997 [7]

—
—
—
—

Giant
Giant
Giant
Giant

Residual aneurysm
Residual aneurysm
Residual aneurysm
Residual aneurysm

—
—
—
—

12—20 monthsb
12—20 monthsb
12—20 monthsb
12—20 monthsb

Partially thrombosed aneurysm
Partially thrombosed aneurysm
Partially thrombosed aneurysm
Partially thrombosed aneurysm

Hodgson et al., 1998 [8]Middle cerebral artery

Small

Residual aneurysm

Residual aneurysm

18 months

Eskridge et al., 1998 [9]

—
—

Giant
Large

—
—

—
—

31—90 days
91—365 days

Murayama et al., 1999 [10]Posteriorcommunicating artery
Superior cerebellar
artery—Large

Residual aneurysm

Residual aneurysm

3 years

Giant

Residual aneurysm—

4 hours—

Residual aneurysm

—

—

—

—

Residual aneurysm

—

—

—

—

Residual aneurysm——

Gruber et al., 1999 [11]Johnston et al., 2000 [12]Description

New compressive symptoms
during follow-up period
New compressive symptoms
during follow-up period

Basilar tip

Giant

Residual aneurysm—

8 months——

Residual aneurysm—

7 months

Horowitz et al., 2002 [15]Anterior
communicating artery
—

Small

Residual neck

Residual aneurysm

23 months———

2 months

Gonzalez et al., 2004 [17]

—
—

Giant
Large

Residual neckComplete occlusion—
Residual aneurysm

8 months
13 months

van Rooij et Sluzewski, 2006 [18]

—

—

—

—

—

Standhardt et al., 2008 [19]Vertebrobasilar
junction
Basilar tip

Giant

Residual neck

Residual aneurysm

4 years

Partially thrombosed aneurysm

Giant

Residual aneurysm

Residual aneurysm

21 months

Partially thrombosed aneurysm

—
—

—
—

—
—

—
—

—
—

Stent-assisted coiling

Pyysalo et al., 2010 [21]

—

Large

Residual aneurysm—

7 years

Present case

Basilar tip

Small

Residual neck

Residual neck

22 months

Piotin et al., 2010 [20]—: Data not described in report.
a Angiographic results at initial embolization and time of rupture classiﬁed according to the Montreal Scale.
b Used because no precise description given in report.

A. Tsurumi et al.

Birchall et al., 2001 [13]Ng et al., 2002 [14]Brilstra et al., 2004 [16]56Table 1

Delayed rupture of saccular coil-packed aneurysm

57

Figure 2 Preoperative three-dimensional digital subtraction angiography, anteroposterior view (A) and rostrocaudal view (B).
Right vertebral angiography, anteroposterior view (C) and lateral view (D), shows a basilar tip aneurysm 7.4 mm in diameter. Right
vertebral angiography just after the initial saccular coiling shows 95% neck-remnant occlusion of the aneurysm (E).

developed new compressive symptoms in the postoperative
follow-up period prior to rupture of the aneurysm. Symptomatic aneurysms, which suggest recent growth and wall
instability [22], could be associated with an increased riskof delayed rupture.
In addition, 16 delayed ruptures occurred in large andgiant aneurysms, while only two were associated with small
aneurysms. A high aspect ratio (dome-to-neck ratio) correlates with aneurysm rupture [23]. Large and giant aneurysms
tend to have a high aspect ratio and should therefore receive
particular attention even after coiling.
All reported cases of delayed rupture of previously unruptured aneurysms after saccular coil packing were seen in

aneurysms with dome ﬁlling (residual aneurysm) [24,25],
and 17 of the 26 aneurysms were incompletely occluded(residual aneurysm) at the time of initial embolization.
Three aneurysms were subtotally occluded (residual neck)at the time of initial embolization; however, coil compaction
and dome ﬁlling of the aneurysm were revealed on follow-up
cerebral angiography. No descriptions regarding the degreeof occlusion were given in the other six cases, and no cases(except for the present case) ruptured without dome ﬁlling.
Rupture occurs preferentially at the site of the aneurysm
dome [23]; thus, a completely occluded or neck-remnantoccluded aneurysm may be considered relatively safe forthe prevention of aneurysm rupture.

58

A. Tsurumi et al.

Figure 3

Computed tomography performed on the day after initial embolization shows no intracranial hemorrhage.

Delayed rupture after ﬂow-diversion treatment

Figure 4 Follow-up magnetic resonance angiography done
6 months after initial embolization shows complete occlusionof the aneurysm.

Flow diverters are increasingly being used for the treatment of wide-necked cerebral aneurysms, and delayed
rupture of the treated unruptured aneurysm after ﬂowdiverter implantation has been reported in some studies[26]. The mechanisms of delayed rupture after such treatment are probably different from those following saccularcoiling. In our review of the literature, the time delay
between saccular coiling and rupture ranged from 4 hours
to 7 years. Most ruptures (18 out of 20) happened more than
3 months after embolization (Table 1). In contrast, Kulcsar
et al. [22] reported that delayed rupture after ﬂow-diverter
treatment occurred more frequently within 3 months oftreatment: there were ten early (< 3 months) ruptures andthree late (3—5 months) ruptures among 13 delayed-rupturecases reported in patients with previously unruptured cerebral aneurysms treated with a ﬂow diverter.
Implantation of a ﬂow diverter led to signiﬁcant ﬂow
changes around the aneurysm; however, inﬂow jets werestill present immediately after treatment in most patientswith delayed rupture [22]. Computational ﬂuid dynamics
analysis of cerebral aneurysms that ruptured after the
deployment of ﬂow diverters revealed that placement of

Figure 5 Follow-up magnetic resonance angiography performed 18 months after initial embolization shows small recanalization
at the neck of the aneurysm.

Delayed rupture of saccular coil-packed aneurysm

59

Figure 6 A. Computed tomography taken on the day of onset of loss of consciousness shows Fisher group 3 subarachnoid hemorrhage. B—D. Emergency three-dimensional digital subtraction angiography, anteroposterior (B) and lateral (C) views, and rightvertebral angiography (D) carried out on the day of onset shows a small recurrence on the ventral part of the aneurysm neck.
E. Complete obliteration of the aneurysm was achieved using a stent-assisted coiling technique.

the device could increase intra-aneurysm pressure, thereby
potentially causing rupture of the aneurysm [27].
Another potential mechanism of delayed rupture involves
post-ﬂow- diversion thrombosis of the aneurysm sac. Thrombosis of the sac can activate an inﬂammatory reaction at theaneurysm wall, which can result in weakening of the cerebral aneurysm [28] even though thrombus formation is theﬁrst step towards permanent aneurysm repair through cicatrization and reverse remodeling of the vessel wall. Dual
antiplatelet therapy after ﬂow-diversion treatment could
also play a role in delayed rupture. Most patients treatedwith ﬂow diverters were still taking both aspirin and clopidogrel at the time of rupture [22].

Treatment of recanalized aneurysms
Our present case is the ﬁrst report of delayed rupture dueto the minor recurrence of a previously unruptured small
asymptomatic cerebral aneurysm after saccular coil packing. It indicates that while the risk of bleeding from sucha minor recurrence in a previously unruptured cerebral
aneurysm is far less than that for a previously ruptured cerebral aneurysm [12], bleeding can still occur. Therefore, a
repeat operation should be considered when recurrence of
the aneurysm is detected.
Several treatment strategies can be used for reoperationof aneurysm recurrence, including balloon-neck remodeling, stent-assisted coiling and ﬂow diverters; however,treatment may be difﬁcult in cases with anatomicallycomplex aneurysms, including a small recurrence and/or
a wide neck. The balloon-neck remodeling technique has
equivalent safety and achieves better occlusion comparedwith the standard coiling technique [29]. This meansthat the wider use of the remodeling technique can beproposed not only for recanalized unruptured aneurysms,
but for ruptured/re-ruptured aneurysms as well. Stentassisted coil embolization is another helpful technique forre-embolization of a minor recurrence in a wide-necked
aneurysm [30], and was used to achieve total occlusion in
the present case. However, aneurysm stent placement is60
associated with a higher mortality compared with coilingwith or without balloon-neck remodeling [20]. Accordingly,
the wider use of stents is probably not to be recommended[29]. A ﬂow diverter is yet another option for the initial treatment and retreatment of anatomically complex
aneurysms; however, treatment using ﬂow diverters canbe difﬁcult in the context of dual antiplatelet therapy,
particularly for ruptured/re-ruptured aneurysms.

Conclusion
The risk of bleeding of a minor recurrence of a previously
unruptured cerebral aneurysm after saccular coil packing is extremely low. The presence of dome-ﬁlling after
coil embolization, symptomatic aneurysms and large/giant
aneurysms all increase the risk of delayed rupture in suchcoil-packed, previously unruptured aneurysms at usuallymore than 3 months after coil embolization.

Disclosure of interest
The authors declare that they have no conﬂicts of interest
concerning this article.

Acknowledgments
The authors thank Dr. Tatsuo Takahashi, Dr. Motoki Oheda,
Dr. Yosuke Tamari, Dr. Tetsuya Tsukada, and Dr. Takayuki
Awaya (Department of Neurosurgery, Nagoya Medical Center) for their helpful discussion.

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