Journal of Clinical Neuroscience 22 (2015) 105–110

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Clinical Study

Intra-aneurysmal thrombus modification after flow-diversion Mario Zanaty, Pascal M. Jabbour ⇑, Roula Bou Sader, Nohra Chalouhi, Stavropoula Tjoumakaris, Robert H. Rosenwasser, L. Fernando Gonzalez Department of Neurosurgery, Thomas Jefferson University and Jefferson Hospital for Neuroscience, 901 Walnut Street, 3rd Floor, Philadelphia, PA 19107, USA

a r t i c l e

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Article history: Received 21 May 2014 Accepted 28 May 2014

Keywords: Flow-diversion Giant aneurysms Intracranial aneurysms Large aneurysms Partially thrombosed aneurysms Pipeline Embolization Device Thrombi

a b s t r a c t Flow diversion has been successfully used to treat large and giant intracranial aneurysms that present with mass effect. We conducted a retrospective review, evaluating the modification of thrombi in this aneurysm type after treatment with the Pipeline Embolization Device (ev3 Endovascular, Plymouth, MN, USA) and the effects of these modifications on symptoms. Eight patients, seven of whom were female, harbored eight partially thrombosed large or giant aneurysms. Five of the eight aneurysms presented with symptomatic mass effect. At 1 year follow-up, complete occlusion occurred in 75% (6/8) of patients. On average, the longest thrombus diameter measured 22.31 mm before treatment and 14.05 mm 1 year afterwards. Seven of the eight thrombi regressed, as did their aneurysms. All six patients with shrunken thrombi had tremendous symptom improvement and became asymptomatic in the following year. The current findings seem to reflect the size variation of the intra-aneurysmal thrombus rather than the size of the aneurysm itself. Ó 2014 Elsevier Ltd. All rights reserved.

1. Introduction

2. Methods

The flow diversion (FD) technique is a novel endovascular treatment that offers the advantage of exosaccular aneurysmal treatment, in contrast to alternative therapies that rely on endosaccular embolization. This technique allows the exclusion of the aneurysm from the circulation that leads to stasis of blood in the aneurysmal sac, which in turn induces an inflammatory response followed by aneurysm thrombosis and parent vessel remodeling. After FD, the thrombus can organize and retract, leading to shrinkage of the aneurysm sac [1], or under different circumstances, the same thrombus can predispose the aneurysm to rupture [2]. FD has been successfully used to treat large and giant aneurysms that present with mass effect [3–8]. How the aneurysm size, thrombosis, and surrounding edema contributes to the appearance of compressive symptoms is poorly understood. The aim of this study is to evaluate the modification of thrombi in large and giant partially thrombosed aneurysms after treatment with the Pipeline Embolization Device (PED; ev3 Endovascular, Plymouth, MN, USA), and the effect these modifications have on symptoms.

2.1. Study design and population selection

⇑ Corresponding author. Tel.: +1 21 5955 7000; fax: +1 21 5503 7038 E-mail address: [email protected] (P.M. Jabbour). http://dx.doi.org/10.1016/j.jocn.2014.05.033 0967-5868/Ó 2014 Elsevier Ltd. All rights reserved.

We conducted a retrospective review of the clinical charts at our institution of all patients who presented with a large or giant partially thrombosed aneurysm and underwent FD treatment between January 2011 and December 2013. Eight patients constituted the study population. The FD device used was the PED. Indications for FD were recurrence of previously treated aneurysms, presence of multiple comorbidities that contraindicated surgery, difficult-to-clip aneurysms, and wide-necked aneurysms. Informed consent was obtained from all subjects.

2.2. Periprocedural angiographic evaluation All eight patients had undergone cross-sectional studies with MRI and digital subtraction angiography (DSA) before treatment. PED embolization was evaluated as; achieving complete stasis, achieving significant stasis, or achieving no disruption of the inflow jet based on a perioperative angiogram. All patients had a baseline neurologic or neuro-ophthalmologic examination before treatment and at the time of follow-up imaging studies. Clinical and imaging results were documented and evaluated at the time they were obtained.

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2.3. Follow-up/angiographic outcomes Patients were evaluated in the hospital for periprocedural complications. After discharge, patients were scheduled for follow-up imaging that included angiography at 6 months, 6–12 months and >12 months; and T1-weighted and T2-weighted MRI and timeof-flight magnetic resonance angiography at 6 and 12 months.

3. Results 3.1. Patient and aneurysm characteristics The study included eight patients, seven of whom were females, harboring eight partially thrombosed aneurysms. Most of the patients were aged above 65 years with a mean age of 68 years. For the purpose of this study, all included aneurysms were large or giant and partially thrombosed. We identified one paraclinoid aneurysm, one cavernous carotid aneurysm (Fig. 1), one posteroinferior cerebellar artery (PICA) aneurysm, one posterior communicating artery (PCOM) aneurysm, one basilar trunk aneurysm (BT), one carotid ophthalmic aneurysm (Fig. 2) and two vertebral artery

(VA) aneurysms. All the aneurysms were saccular. The mean aneurysm size was 27.9 mm. Three aneurysms were previously treated by stent assisted coiling (SAC). The paraclinoid and the BT aneurysms (Fig. 3) needed three PED each for sufficient neck coverage, while the cavernous carotid aneurysm and one of the VA aneurysms required two PED per aneurysm. For the rest, one PED per aneurysm provided full neck coverage. Five of the eight aneurysms presented with symptomatic mass effect. Both the patient with the cavernous carotid aneurysm and the patient with the carotid ophthalmic aneurysm aneurysm presented with cranial nerve palsies. The patient with the PICA aneurysm suffered from numbness in the lower and upper extremities associated with recurrent dizzy spells. The patient with the paraclinoid aneurysm complained of retro-orbital pain. Finally, the patient with the BT aneurysm presented with paresthesia in the lower extremities. The two VA aneurysms in the study were found incidentally. One patient with a PCOM aneurysm complained of chronic headache that was most probably not linked to the aneurysm. Measurements of each thrombus were recorded using MRI in the anteroposterior, transverse and craniocaudal plane. In each plane, the line that bridges the most distant points of the aneurysm defined the diameter. The longest diameter of all planes defined the thrombus diameter.

Fig. 1. (a, b) Axial MR angiography source image before Pipeline Embolization Device (PED; ev3 Endovascular, Plymouth, MN, USA) embolization showing a giant, partially thrombosed, cavernous aneurysm that had been previously treated with stent assisted coiling. The thrombus measured 12.6 mm. The aneurysm displays minimal recanalization. 1 year follow-up (c) axial MR angiography source image and (d) sagittal T1-weighted MRI after PED embolization using two devices shows shrinkage of the thrombus in the transverse section (12.1 mm) and other planes (not shown). The recanalization has disappeared.

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Fig. 2. Pre-treatment (a) axial T2-weighted MRI, (b) axial T1-weighted MRI with contrast, (c) axial T1-weighted MRI without contrast, (d, e) coronal T1-weighted MRI with contrast, (f) sagittal T1-weighted MRI with contrast, and (g) axial T2-weighted MRI showing a giant partially thrombosed carotid ophthalmic aneurysm measuring 28.8 (anteroposterior)  18 (transverse)  15.6 (craniocaudal) mm. The thrombus measures 12.5 (anteroposterior)  16 (transverse)  15.6 (craniocaudal) mm. (h, i) 1 year axial follow-up MR angiography source image after placement of three Pipeline Embolization Devices (PED; ev3 Endovascular, Plymouth, MN, USA) shows no gross anomaly adjacent to the site of the devices or the location of the previous aneurysm.

On average, the thrombus diameter was 26.3 mm. Pre- and postPED treatment measurements are listed in Table 1.

by life-long monotherapy with aspirin 81 mg. All patients underwent PED embolization without any periprocedural complication.

3.2. Procedures and periprocedural complications

3.3. Angiographic follow-up

Patients were loaded with 75 mg/day of clopidogrel and 81 mg/ day of aspirin for at least 10 days before the intervention. Dual antiplatelet therapy was envisioned for at least 6 months followed

At 1 year follow-up, complete occlusion occurred in 75% (6/8) of aneurysms as assessed by DSA. The PICA aneurysm and the cavernous aneurysm, which recurred after SAC, were completely

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Fig. 3. Axial (a) T2-weighted MRI and (b) MR angiography source image performed before Pipeline Embolization Device (PED; ev3 Endovascular, Plymouth, MN, USA) embolization showing a giant, partially thrombosed, basilar trunk aneurysm that was previously treated with stent assisted coiling. The thrombus measures 38.1 mm. Axial (c) T2-weighted MRI and (d) MR angiography source image at 3 month follow-up after PED embolization showing shrinkage of the thrombus (now 36.9 mm on axial view) within the aneurysm in all planes.

occluded at 6 month follow-up after PED embolization. The BT aneurysm failed both SAC and PED embolization as evident by the incomplete occlusion on DSA at 1 year follow-up. 3.4. MRI follow-up All thrombi were assessed at 1 year post-treatment using MRI as described in the Method section. We compared the thrombi pre- and post- PED embolization by measuring their size in all three planes. On average, the longest thrombus diameter measured 22.31 mm before treatment and 14.05 mm 1 year afterwards. Seven of the eight thrombi regressed, as did their aneurysms. Furthermore, one thrombus completely disappeared along with its aneurysm. We observed two thrombi that kept growing, even though the aneurysms were completely occluded as demonstrated by DSA. These two thrombi were present in the PICA and PCOM aneurysms. 3.5. Clinical outcome All six patients who had shrunken thrombi had a marked improvement in their symptoms and became asymptomatic at

1 year follow-up. Only one of these six patients, who harbored a carotid cavernous aneurysm, noted a transient worsening of his diplopia after PED placement, and was treated with steroid therapy. Six months later, the same patient noted a significant improvement in his symptoms and became completely asymptomatic by the time of his 1 year follow-up. The patient with an incidental PCOM aneurysm was suffering from chronic headache that got worse in the months following treatment. Lastly, the patient with a PICA aneurysm did not note any improvement in his lower extremity numbness as the thrombus increased in size.

4. Discussion The PED is a promising FD device; it is made of 25% platinum and 75% cobalt-nickel alloy with a pore size ranging from 0.02 to 0.05 mm2 at nominal diameter and offers a high metal coverage (30–35%) of the target vessel [5,6]. PED is currently being used to treat complex, simple, wide-necked, giant, small, fusiform, dissecting, and saccular aneurysms [9]. Of these, large and giant aneurysms pose a challenge for endovascular treatment, tend to present with compression symptoms, and have a high risk of rupture [6]. Treatment is aimed at preventing rupture and decreasing

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M. Zanaty et al. / Journal of Clinical Neuroscience 22 (2015) 105–110 Table 1 Aneurysm and thrombus characteristics Aneurysm location

Aneurysm size (mm)

Clot size prePED (mm)

Clot size post-PED (mm)

Number of PED

Symptoms pretherapy

Symptoms posttherapy

Previously treated?

Aneurysm occlusion

Cavernous aneurysm

AP = 20.2 TR = 13.0 CC = 18.1 AP = 28.8 TR = 18.0 CC = 15.6 AP = 19.1 TR = 19.0 CC = 16.8 AP = 17.2 TR = 12.7 CC = 18.8 AP = 37.3 TR = 30.1 CC = 25.0 AP = 27.8 TR = 29.7 CC = 22.3 AP = 26.5 TR = 40.1 CC = 45.3 AP = 23 TR = 24 CC = 23

AP = 8.5 TR = 12.6 CC = 12.8 AP = 12.5 TR = 16.0 CC = 15.6 AP = 12.0 TR = 17.2 CC = 11.6 AP = 3.3 TR = 10.3 CC = 17.1 AP = 34.3 TR = 28.1 CC = 23.9 AP = 13.4 TR = 11.6 CC = 10 AP = 26.1 TR = 38.1 CC = 45.3 AP = 22.8 TR = 22.3 CC = 22.3

AP = 8.0 TR = 12.1 CC = 13.6 No gross anomaly can be appreciated

2

CN palsy

Complete resolution of symptoms

SAC

CO

3

Retro-orbital pain + headaches

Complete resolution of symptoms

No

CO

AP = 17 TR = 21.5 CC = 22.3 AP = 14.7 TR = 14.2 CC = 19.2 AP = 19 TR = 23.6 CC = 18.8 AP = 12 TR = 13.3 CC = 10 AP = 26 TR = 36.9 CC = 40.6 AP = 22.3 TR = 20.1 CC = 18.4

1

Dizziness, UE and LE numbness

Dizziness with movement

SAC

CO

1

Headaches

Headaches

No

CO

1

CN palsy

Complete resolution of symptoms

No

CO

2

Incidental

_

No

CO

3

Paresthesia

Complete resolution of symptoms

SAC

Incomplete occlusion

1

Incidental

_

Paraclinoid aneurysm PICA aneurysm

PCOM aneurysm

Carotid ophthalmic aneurysm VA aneurysm

Basilar trunk aneurysm VA aneurysm

CO

AP = anteroposterior plane, CC = coronary plane, CN = cranial nerve, CO = complete occlusion, LE = lower extremity, PED = Pipeline Embolization Device (ev3 Endovascular, Plymouth, MN, USA), PCOM = posterior communicating artery, PICA = posterior inferior cerebellar artery, SAC = stent assisted coiling, TR = transverse plane, UE = upper extremity, VA = vertebral artery.

the mass effect. It is thought that symptoms result from a combination of edema surrounding the artery, intra-aneurysmal thrombus and aneurysm pulsation. SAC and balloon assisted coiling were developed to deal with such complex aneurysms, but have a high rate of recanalization [10–13]. Furthermore, if this technique fails to disconnect the aneurysm from the circulation, pulsation will continue to be transmitted through the sac and symptoms will remain [14–16]. Additionally, FD treatment offers the advantage of avoiding coil insertion that may worsen the pre-existing mass effect. Therefore, PED embolization is a rational option for treating symptomatic large and giant partially thrombosed aneurysms. Lylyk et al. [5] and Szikora et al. [17] reported an improvement of mass effect symptoms after FD treatment. Piano et al. found that 61% of the aneurysms shrank after FD. However, the results are not always favorable; the inflammatory changes inside the aneurysm may cause a transient worsening of the mass effect by increasing the aneurysm size [5], or perhaps by direct spread of the inflammation to the surrounding parenchyma [18]. This worsening of symptoms is usually seen early after the procedure. The present report focuses on the alteration of intra-aneurysmal thrombus after FD, and the effect this alteration has on patient symptoms. The MRI at 6 months and 1 year follow-up demonstrated that 75% (6/8) of the aneurysms in our study had a reduction in the size of their thrombi, and all of them were completely occluded on angiography. All six aneurysms that showed a decrease in size of the intra-aneurysmal thrombus were no longer symptomatic, despite the fact that one of the aneurysms was not completely occluded (

Intra-aneurysmal thrombus modification after flow-diversion.

Flow diversion has been successfully used to treat large and giant intracranial aneurysms that present with mass effect. We conducted a retrospective ...
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