Keywords

Patient

A 75-year-old female patient with an anxiety disorder but with an otherwise insignificant medical history underwent an MRI examination as work-up for recurrent headaches. A large aneurysm of the left middle cerebral artery (MCA) bifurcation was found. The said aneurysm was treated by endovascular means. Her headaches did not improve after the aneurysm treatment; however, they disappeared after a course of high-dosage steroids was begun, supporting the diagnosis of a giant cell arteritis. During the following long-term course, repeated coil treatment sessions were carried out on the aneurysm. At the age of 82 years, she presented after a short episode of impaired consciousness and poor articulation, which might well have been the expression of an epileptic seizure. These symptoms were considered indirectly related to a recurrence of the previously coiled aneurysm.

Diagnostic Imaging

CT/CTA and MRI/MRA were carried out in December 2011 and showed a large wide-necked aneurysm of the left MCA bifurcation (neck width 5.5 mm, fundus width 13 mm, fundus depth 7 mm). Further aneurysms were ruled out. The left Internal Carotid Artery (ICA) was not particularly elongated (Fig. 1).

Fig. 1
figure 1figure 1

Diagnostic imaging in an incidental, large, wide-necked aneurysm of the left MCA bifurcation. Non-contrast cranial CT (a), axial (b) and sagittal (c) contrast-enhanced CT images, DSA in a straight lateral projection (d), and 3D reconstructions of a rotational DSA showing the anterior (e) and posterior aspect (f) of said aneurysm

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Treatment Strategy

The main goal of the treatment was to prevent further growth of the aneurysm and possible aneurysm rupture. The following options were explained to the patient and her daughter in a balanced way:

  • Conservative management with annual follow-up imaging and treatment once growth and/or a change of shape has been observed

  • Microsurgical clipping

  • Endovascular coil occlusion, most likely with stent assistance

After thinking through these possibilities, the patient and her family opted for endovascular treatment. It was decided to implant the stents and occlude the aneurysm with coils in separate sessions.

Treatment

Procedure #1, 07.12.2011: endovascular implantation of crossing stents as preparation for assisted coil occlusion of an incidental, wide-necked left MCA bifurcation aneurysm

Anesthesia: general anesthesia, 1× 5,000 IU non-fractionated heparin (Heparin-Natrium, B. Braun) IV, 1× 500 mg ASA (Aspirin I.V. 500 mg, Bayer Vital) IV, 2× 2 mg glyceryl trinitrate (Nitrolingual, G. Pohl-Boskamp) IA

Premedication: 1× 100 mg ASA (Aspirin, Bayer Vital) PO daily and 1× 75 mg clopidogrel (Plavix, Sanofi-Aventis) PO given 5 days before the procedure; Multiplate (Roche Diagnostics) (ARU): ADP 39, ASPI 56 (dual platelet function inhibition)

Access: right common femoral artery, long 8F sheath (St. Jude); guide catheter: 8F Guider Softip (Boston Scientific); intermediate catheter: DAC (Concentric); microcatheter: 1× Prowler Select Plus J (Cerenovus); microguidewire: 0.016” Radifocus Guidewire GT (Terumo)

Implants: 2× Solitaire SAB 3/30 (Medtronic)

Course of treatment: an 8F guiding catheter and an intermediate catheter were inserted into the left ICA. The inferior trunk of the left MCA was catheterized without difficulty, and a Solitaire stent was implanted from this vessel to the left M1 segment. After the stent had been detached, the same microcatheter was used to catheterize the superior trunk of the left MCA. From there, a second Solitaire stent was implanted into the left M1 segment, crossing the first stent (Fig. 2).

Fig. 2
figure 2

Preparation for coil occlusion of a wide-necked left MCA bifurcation aneurysm by implanting two Solitaire stents. The first stent was implanted from the inferior trunk (distal markers, yellow arrow (a)); the second stent was deployed from the superior trunk (distal markers, blue arrow (b)). Both stents cross each other in front of the aneurysm and the proximal ends are deployed into one another in the left M1 segment

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Duration: 1st–10th run: 56 min; fluoroscopy time: 25 min

Complications: none

Postmedication: 1× 100 mg ASA PO for life and 1× 75 mg clopidogrel PO daily for at least 3 months

Procedure #2, 13.01.2012: endovascular coil occlusion of a wide-necked left MCA bifurcation aneurysm after preparatory implantation of crossing stents 5 weeks previously

Anesthesia: general anesthesia, 1× 5,000 IU non-fractionated heparin (Heparin-Natrium, B. Braun) IV, 1× 500 mg ASA (Aspirin i.v. 500 mg, Bayer Vital) IV, 1× 2 mg glycerol trinitrate (Nitrolingual, G. Pohl-Boskamp) IA

Premedication: 1× 100 mg ASA PO daily and 1× 75 mg clopidogrel PO daily for the last 6 weeks

Access: right common femoral artery, long 8F sheath (St. Jude); guide catheter: 8F Guider Softip (Boston Scientific); intermediate catheter: ReFlex 058 (Reverse Medical); microcatheter: 1× Echelon 10 90°, 1× Echelon 10 straight (Medtronic); microguidewire: 0.014″ Transend ex (Stryker)

Implants: 18 coils: 1× Nexus Helix Soft 10/30 (ev3), DeltaPlush Cerecyte 1× 4/8, 6× 4/6, 5× 3/6, 1× 3/4, 4× 2/6 (Codman)

Course of treatment: after access to the left ICA, the MCA aneurysm was catheterized with an Echelon 10 microcatheter through the crossed Solitaire stents. Despite these stents, coil retention inside the aneurysm was not particularly stable. A partial coil occlusion was achieved, and the decision was made to wait for several weeks for the necessary completion of the coil occlusion (Fig. 3).

Fig. 3
figure 3

Partial coil occlusion of a wide-necked left MCA aneurysm after preparatory implantation of crossing stents. A working projection was chosen which showed the aneurysm neck free from the superimposition of the efferent MCA branches (a). A microcatheter with a 90° angled tip was inserted (b). Inserting the coils was more difficult than expected, and the poor coil retention exerted by the crossing stents did not allow for a complete occlusion of the aneurysm (c, d)

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Duration: 1st–37th run: 201 min; fluoroscopy time: 107 min

Complications: transient right-hand hemiparesis and aphasia, which resolved within 2 days and was considered to be a sequel of contrast medium toxicity

Postmedication: 1× 100 mg ASA PO for life and 1× 75 mg clopidogrel PO daily for at least 1 year

Procedure #3, 01.03.2012: completion of the endovascular coil occlusion of a wide-necked left MCA bifurcation aneurysm after preparatory implantation of crossing stents and after previous partial coil occlusion

Anesthesia: general anesthesia, 1× 5,000 IU non-fractionated heparin (Heparin-Natrium, B. Braun) IV, 1× 2 mg glycerol trinitrate (Nitrolingual, G. Pohl-Boskamp) IA

Premedication: 1× 100 mg ASA PO daily and 1× 75 mg clopidogrel PO daily since December 2011

Access: right common femoral artery, long 8F sheath (St. Jude); guide catheter: 8F Guider Softip (Boston Scientific); intermediate catheter: ReFlex 058 (Reverse Medical); microcatheter: 1× Excelsior SL10 straight (Stryker); microguidewire: 0.014″ Traxcess 14 (MicroVention)

Implants: 15 coils: 5× Standard Fiber 3/10 (ev3), 1× Standard Fiber 2/6, not insertable (ev3), DeltaPlush Cerecyte 2× 2/6, 7× 2.4/4 (Codman)

Course of treatment: after access to the left ICA, the left MCA aneurysm was catheterized. Coil insertion was much easier than during the previous session, and the 14 coils implanted allowed for a sufficiently occluded aneurysm with a neck remnant (Fig. 4).

Fig. 4
figure 4

Completion of the coil occlusion of a wide-necked left MCA bifurcation aneurysm. A previous treatment session 6 weeks earlier resulted in a partial coil occlusion (a). Inserting a further 14 coils resulted in a densely packed aneurysm with a non-occluded neck (b). This neck was most likely the reason for the reperfusion of the aneurysm

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Duration: 1st–12th run: 143 min; fluoroscopy time: 105 min

Complications: none

Postmedication: 1× 100 mg ASA PO for life and 1× 75 mg clopidogrel PO daily for 1 year

Procedure #4, 14.06.2012: completion of endovascular coil occlusion of a wide-necked left MCA bifurcation aneurysm after preparatory surgery where crossing stents were implanted and after two previous coiling sessions

Anesthesia: general anesthesia, 1× 5,000 IU non-fractionated heparin (Heparin Natrium, B. Braun) IV

Premedication: 1× 100 mg ASA PO daily and 1× 75 mg clopidogrel PO daily since December 2011

Access: right common femoral artery, long 8F sheath (St. Jude); guide catheter: 8F Guider Softip (Boston Scientific); intermediate catheter: ReFlex 058 (Reverse Medical); microcatheter: 1× Excelsior SL10 straight (Stryker); microguidewire: 0.014″ Traxcess 14 (MicroVention)

Implants: 8 coils: DeltaPlush Cerecyte 6× 3/6, 2× 2/4 (Codman)

Course of treatment: the left MCA aneurysm was catheterized again. A total of eight coils were implanted (Fig. 5).

Fig. 5
figure 5

Fourth treatment session with coil occlusion of a partially recanalized wide-necked left MCA bifurcation aneurysm, pre (a) and post (b) recoiling, required 5 months after the first coiling session

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Duration: 1st–9th run: 62 min; fluoroscopy time: 31 min

Complications: none

Postmedication: 1× 100 mg ASA PO for life and 1× 75 mg clopidogrel PO daily for 1 year

Clinical Outcome

After the second procedure, the patient developed temporary aphasia and hemiparesis of the right side, which both resolved within 2 days. CT right after the patient woke up from general anesthesia showed swelling and contrast medium accumulation in the left MCA supply territory, which resolved alongside the clinical symptoms within 2 days (Fig. 6).

Fig. 6
figure 6

NCCT after the coil occlusion of a left MCA bifurcation aneurysm. The patient woke up from anesthesia with aphasia and hemiparesis on the right side. NCCT showed a swelling and contrast medium accumulation of the left MCA supply territory (a), which resolved within 2 days (b). Contrast medium toxicity and relative hypoperfusion during coil insertion were considered the most likely reasons for the transient neurological deficit

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Follow-Up Examinations

Follow-up DSA 17 months after the first and 12 months after the third coiling session confirmed complete aneurysm occlusion. However, just 1 year later, DSA once again showed a reperfusion of the aneurysm (Fig. 7).

Fig. 7
figure 7

Follow-up DSA 1 year after the so far last coiling session showed a complete occlusion of the aneurysm (a). Only 1 year later, the aneurysm was once again partially recanalized (arrows (b, c))

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Treatment Strategy

A continuation of the treatment was considered crucial. The surgical creation of an extracranial-intracranial bypass between the superficial temporal artery and the left-hand MCA, followed by the parent vessel occlusion at the level of the MCA bifurcation, was discussed with the patient. She did not want to have any open surgery. We therefore offered another endovascular treatment session.

Treatment

Procedure #5, 20.06.2014: completion of the endovascular coil occlusion of a wide-necked left MCA bifurcation aneurysm after preparatory implantation of crossing stents and after three previous coiling sessions

Anesthesia: general anesthesia, 1× 3,000 IU non-fractionated heparin (Heparin-Natrium, B. Braun) IV, 1 mg glycerol trinitrate IA

Premedication: 1× 100 mg ASA PO daily and 1× 75 mg clopidogrel PO daily since December 2011

Access: right common femoral artery, 6F sheath (Terumo); guide catheter: 6F Guider Softip (Boston Scientific); microcatheter: 1× Excelsior SL10 straight (Stryker); microguidewire: Synchro 14 (Stryker)

Implants: 9 coils: DeltaPlush Cerecyte 1× 6/25 (Codman), HydroCoils 2× 5/15, 2× 4/10, 1× 3/10, 1× 3/6, MicroPlex10 1× 3/8, 1× 2/6 (MicroVention)

Course of treatment: the left MCA aneurysm was catheterized, and a total of nine coils were implanted (Fig. 8).

Fig. 8
figure 8

Fifth treatment session with repeated coil occlusion of a partially recanalized wide-necked left MCA bifurcation aneurysm, pre (a), during (b), and after (c) recoiling, required 23 months after the first coiling session

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Duration: 1st–9th run: 109 min; fluoroscopy time: 60 min

Complications: none

Postmedication: 1× 100 mg ASA PO for life and 1× 75 mg clopidogrel PO daily for 1 year

Follow-Up Examinations

Follow-up DSA 1 year later or 3.5 years after the first coiling session again showed a reperfusion of the aneurysm. The patient did, however, not accept the proposal of new treatment (Fig. 9).

Fig. 9
figure 9

Partial reperfusion of a wide-necked left MCA bifurcation aneurysm after five previous procedures. The recanalization has reached the aneurysm wall (arrow)

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The next follow-up examinations were carried out 4 years later, when the patient presented after a short episode of disturbed consciousness and poor articulation. CT showed massive edema of the white matter of the left temporal lobe. DSA revealed a recanalization of the aneurysm between the coil loops. The maximum diameter of the aneurysm had increased if compared to the initial diameter, but the coil mass was still compact. MRI and DSA only 2 months later showed a rapid further increase in the size of the aneurysm. The perfused part of the aneurysm was embedded in a huge aneurysm sac filled with thrombus and with intense contrast enhancement of the aneurysm wall (Fig. 10).

Fig. 10
figure 10figure 10

Long-term follow-up 7.5 years after the initial endovascular treatment of a wide-necked left MCA bifurcation aneurysm. The patient was symptomatic with a transient episode of disturbed consciousness and impaired articulation. CT (a) showed a massive edema of the left temporal lobe and DSA (b) revealed an increased reperfusion of the coiled aneurysm between the coil loops. Only 2 months later, the aneurysm sac had increased to a maximum diameter of 36 mm (c), the edema had also increased (d), and there was an intense contrast enhancement of the aneurysm wall (e). The coil loops had migrated into the thrombus within a short period and a lumen with a spherical shape had reperfused (f, g)

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Treatment Strategy

The failure of the endovascular treatments to prevent this aneurysm from growing was obvious. Conservative management would have been associated with a foreseeable risk of further growth. Microsurgical clipping or the creation of an extra-intracranial bypass, followed by occluding the left MCA bifurcation, was again discussed. The anticipated risks were considered high, and the patient was not willing to undergo open surgery. Knowing the presumably limited efficacy further coil occlusion was offered to and accepted by the patient.

Treatment

Procedure #6, 07.10.2019: repeated endovascular stent-assisted coil occlusion of an incidental, wide-necked left MCA bifurcation aneurysm

Anesthesia: general anesthesia, 3,000 IU unfractionated heparin (Heparin-Natrium, B. Braun) IV

Premedication: the patient had been under dual platelet function inhibition since December 2011 but had stopped this medication in mid-2018; dual platelet inhibition was reinstituted 5 days before this treatment by a medication of 1× 100 mg ASA PO daily and 2× 90 mg ticagrelor PO daily. A Multiplate Analyzer test (Roche Diagnostics) confirmed significant dual platelet function inhibition.

Access: right common femoral artery, 1× 6F sheath (Terumo); guide catheter: 1× 6F Heartrail II (Terumo); microcatheter: 1× Excelsior SL 10 45° (Stryker); microguidewire: 1× pORTAL 0.014″ 200 cm (phenox)

Implants: 10 coils: 5× Target XL 360° Soft 5/10, 2× Target XL 360° Soft 2/6, 3× Target XL 360° Soft 2/3 (Stryker)

Course of treatment: the guiding catheter was placed in the midcervical segment of the left ICA, followed by an atraumatic navigation of the Excelsior microcatheter into the reperfused coil mass. The aforementioned coils were placed one by one into the aneurysm. A final DSA run confirmed the complete occlusion of the perfused part of the aneurysm (Fig. 11).

Fig. 11
figure 11

Retreatment of a recurrent perfusion of a left MCA bifurcation aneurysm. The previously implanted coils have separated due to coil migration into the intraaneurysmal thrombus (arrow (a, b). Another ten coils were inserted to obliterate this compartment of the aneurysm (c)

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Duration: 1st–12th DSA run: 63 min; fluoroscopy time: 32 min

Complications: none

Postmedication: 1× 100 mg ASA PO daily, 3× 4 mg dexamethasone (Fortecortin, Merck Serono) PO daily for 10 days, 60 mg etoricoxib (Arcoxia, MSD Sharp & Dohme) for 6 weeks

Follow-Up Examinations

Immediate postprocedural MRI showed that the size of the aneurysm and the edema remained unchanged (Fig. 12).

Fig. 12
figure 12

FLAIR MRI after the coil treatment of a retreated, partially thrombosed left MCA aneurysm with significant edema of the adjacent left temporal and occipital lobe

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Clinical Outcome

The patient tolerated the endovascular treatment sessions well. Her clinical condition at the latest discharge was mRS 1 with mild chronic cognitive impairment.

Discussion

This failure of endovascular coil occlusion to permanently exclude an intracranial aneurysm from the blood circulation is the rare exception. This may not only result in the rupture of said aneurysm. Further aneurysm growth and perianeurysmal edema are also possible sequelae. Perianeurysmal edema is a not very well-understood phenomenon and has been described with both treated and untreated cerebral aneurysms (Fanning et al. 2008; Su et al. 2014). The reported incidence varies from about 1% in the total population of endovascular-treated patients (Sim et al. 2015) up to 95% in highly selected cases (Krings et al. 2007), where almost all (17 of 18) of untreated, large or giant, partially thrombosed aneurysms showed perianeurysmal edema. Luckily, the majority of the patients is asymptomatic for the perianeurysmal edema. Only a few cases have been published where patients have suffered from seizures, hydrocephalus, or neurological deterioration due to the edema.

It is still unknown which aneurysm is more likely to show perianeurysmal edema, because there is no favored location. However, if the aneurysm is large or partially thrombosed, perianeurysmal edema is more likely. Aneurysms with edema are often embedded in the brain parenchyma, although it seems that direct contact between the aneurysm wall and the brain parenchyma is needed, as shown by Dengler et al. (2015). In their series, giant cavernous ICA aneurysms which were separated from the brain by dura mater did not cause any perianeurysmal edema, even though they exerted mass effect and brain indentation.

Since perianeurysmal edema is found in different cases, there might be more than one underlying mechanism (e.g., arterial hypertension, Lukic et al. 2015). Mass effect is one, as in large or giant aneurysms perianeurysmal edema is seen more frequently. A water hammer effect has also been proposed. Partially (re)perfused aneurysms (Tomokiyo et al. 2007) and intraaneurysmal thrombus (Roccatagliata et al. 2010) or recurrent hemorrhage in the aneurysm wall, especially giant or partially thrombosed aneurysms, may play a role (Krings et al. 2007). With its inflammatory mediators, cytokines and pro-inflammatory substances (Frösen et al. 2012; Sim et al. 2015) may contribute. In aneurysms with perianeurysmal edema, contrast enhancement of the aneurysm wall can almost always be observed (Su et al. 2014). This may suggest that there is an underlying inflammatory process. Perianeurysmal edema is usually vasogenic, not cytotoxic.

As several studies have shown, aneurysmal wall enhancement is associated with a higher risk of aneurysm instability (Vergouwen et al. 2019), meaning growth, rupture (Sato et al. 2019; Frösen et al. 2012), or recurrence after treatment (Fanning et al. 2008). Partially thrombosed aneurysms show not only a higher risk of treatment-related complications but also a higher risk of growth and rupture if left untreated (Sano et al. 1998).

Like in the case presented above, Hasan et al. (2012) showed in a case series of eight major recurrences after coil embolization that aneurysm sac growth rather than coil compaction was the primary mechanism associated with aneurysm recurrence. In our patient, coil migration into the intraaneurysmal thrombus occurred in addition.

Although per se asymptomatic in the majority of cases, perianeurysmal edema around treated aneurysms is considered a warning sign, possibly indicating recurrent aneurysm perfusion with the risk of further aneurysm growth and rupture.

Cross-References