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UvA-DARE (Digital Academic Repository)

Durability of endovascular treatment for intracranial aneurysms

Ferns, S.P.

Publication date

2010

Document Version

Final published version

Link to publication

Citation for published version (APA):

Ferns, S. P. (2010). Durability of endovascular treatment for intracranial aneurysms.

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Durability of

enDovascular treatment

for intracranial

aneurysms

uitnoDiGinG

voor het bijwonen van de openbare verdediging van het proefschrift

Durability of endovascular

treatment for

Intracranial aneurysms

door

Sandra P. Ferns

op dinsdag 12 oktober 2010 om 14.00 uur in de agnietenkapel oudezijds voorburgwal 231 1012 eZ amsterdam Receptie na afloop van de promotie ter plaatse

Paranimfen sanna Gevers s.gevers@amc.uva.nl Debbie ferns debbieferns@gmail.com sandra P. ferns Plantage Parklaan 24-ii 1018 sv amsterdam s.p.ferns@amc.uva.nl

tram: 4, 9, 16, 24, 25 halte spui

Durability of en

D

ov

ascular trea

tment for intracranial aneur

ysms

s

.p

.

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This thesis was prepared at the departments of Radiology, Academic Medical Center, University of Amsterdam, and St. Elisabeth Ziekenhuis Tilburg, both in the Netherlands Copyright © 2010, Sandra Pauline Ferns, Amsterdam, the Netherlands

No part of this thesis may be reproduced, stored or transmitted in any form or by any means, without prior permission of the author.

The research described in this thesis was financially supported by the Nuts Ohra Foundation (SNO0602-22), the Netherlands, and the Netherlands Brain Foundation (15F07.12)

Printing of this thesis was financially supported by:

Department of Radiology, Academic Medical Center Amsterdam, the Netherlands

Cover: Jeroen Henneman ‘Het beroemde potlood’ (1998) Printed by: Gildeprint Drukkerijen

Lay out: Bread and pepper webdesign, www.breadandpepper.nl ISBN: 978-90-9025636-8

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DURABILITY OF ENDOVASCULAR TREATMENT

FOR INTRACRANIAL ANEURYSMS

ACADEMISCH PROEFSCHRIFT ter verkrijging van de graad van doctor

aan de Universiteit van Amsterdam op gezag van de rector magnificus

prof. dr. D.C. van den Boom

ten overstaan van een door het college voor promoties ingestelde commissie, in het openbaar te verdedigen in de Agnietenkapel

op 12 oktober 2010, te 14.00 uur

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Promotor: Co-promotores:

Overige leden:

Promotiecommissie: Prof. dr. W.J.J. van Rooij dr. C.B.L.M. Majoie dr. M.E.S. Sprengers dr. R. van den Berg Prof. dr. G.J. den Heeten Prof. dr. J.J. van Overbeeke Prof. dr. J.A. Reekers Prof. dr. J. Stam

Prof. dr. W.P. Vandertop Dr. A. van der Lugt Faculteit der Geneeskunde

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TABLE OF CONTENTS

Chapter 1 9

Introduction and outline of the thesis

Chapter 2 17

Coiling of intracranial aneurysms: A systematic review on initial occlusion and reopening and retreatment rates.

Stroke 2009

Chapter 3 41

Late reopening of adequately coiled intracranial aneurysms: frequency and risk factors in 400 patients with 440 aneurysms.

In press

Chapter 4 59

De novo aneurysm formation and growth of untreated aneurysms: 5-year MRA follow-up in a large cohort of patients with coiled aneurysms and review of the literature.

In press

Chapter 5 75

Long term MRA follow-up after coiling of intracranial aneurysms: impact on mood and anxiety.

Neuroradiology 2010

Chapter 6 93

Late adverse events in coiled ruptured aneurysms with incomplete occlusion at 6 months angiographic follow-up.

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chapter 7 113 Partially thrombosed intracranial aneurysms presenting with

mass effect: Long-term clinical and imaging follow-up after endovascular treatment.

AJNR Am J Neuroradiol 2010

chapter 8 137

Summary of findings and implications

Samenvatting in het Nederlands 146

List of Abbreviations 152

List of publications 156

Dankwoord 157

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1

Introduction and outline

of the thesis

1

Introduction and outline

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Durability of endovascular treatment for intracranial aneurysms

10

introDuction

intracranial aneurysms

Intracranial aneurysms are intimal outpouchings due to focal weakness of the medial layer of the vessel wall of cerebral arteries, and are present in 0.4 to 6% of the general population.1 In a small number of patients, intracranial aneurysms rupture, causing a bleeding in the brain (subarachnoid hemorrhage or SAH) with high morbidity and mortality rates. Annual incidence of SAH from an intracranial aneurysm is estimated to be 0.04-1.2%, leading to approximately 1200 hospital admissions due to SAH per year in the Netherlands (source: Netherlands Heart Foundation 2004).2-4 Early securing of the aneurysm is vital to prevent a frequently fatal early recurrent hemorrhage.

Diagnosis and treatment

Intracranial aneurysms are mostly discovered during imaging work-up in the acute situation of a SAH by Computed Tomography Angiography (CTA), Magnetic Resonance Angiography (MRA) or Digital Subtraction Angiography (DSA). Unruptured aneurysms may be found as additional aneurysms in patients with another ruptured aneurysm, in patients presenting with neurologic symptoms due to mass effect, or be found incidentally.

For long, the standard treatment for intracranial aneurysms was to place a micro-neurosurgical clip over the aneurysm neck, excluding the aneurysm from the circulation with the goal to prevent a (recurrent) hemorrhage. In the early ‘90s, an endovascular approach has been developed.6 The introduction of micro catheters and a detachable

coil system allowed the operator to selectively catheterize the aneurysm and fill the aneurysm lumen with platinum coils to prevent recurrent hemorrhage. Aneurysm coiling has gradually replaced surgery as the first line treatment of choice, since, in 2002, a large multicenter randomized controlled trial showed that patients had better short-term outcome after coiling compared to clipping.7

Although coiling has become the preferred treatment for both ruptured and unruptured intracranial aneurysms, and clipping has become only indicated for aneurysms not suitable for coiling, it has several shortcomings. First, not all aneurysms can be completely occluded at first treatment, leaving the patient at risk for early recurrent hemorrhage. Second, a substantial part of coiled aneurysms shows instability with time. Aneurysms may reopen due to coil compaction, growth of the aneurysm, coil migration into intraluminal thrombus, or dissolving of intraluminal thrombus.8-11

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Introduction and outline of the thesis

Chapter 1

11

imaging follow-up

To assess aneurysm occlusion and discover possible reopening, it is important to perform imaging follow-up in patients with coiled intracranial aneurysms. Aneurysm occlusion is commonly described in a 3-point scale (complete, near-complete with a remaining small neck remnant and incomplete) or in a 2-point scale (adequate and incomplete occlusion), where no distinction is made between complete and near-complete occlusion.12 Incomplete aneurysm occlusion leaves the patient at risk for a

SAH, and retreatment is often advocated.

Possible determinants for initial incomplete aneurysm occlusion are unfavorable aneurysm anatomy and vessel geometry and types of coils that are used. Possible risk factors for reopening of a coiled aneurysm over time are large aneurysm size, presence of intraluminal thrombus, low packing density, initial incomplete occlusion, duration of follow-up, ruptured aneurysms, location in the posterior circulation, and a large neck–dome ratio.8,13-17 The magnitude of separate contributions of these risk factors to

aneurysm reopening are not clear, since studies differ in design, selection of aneurysms and method of follow-up.

Longer time after treatment as a risk factor for aneurysm reopening is under debate. Some studies reported more first-time aneurysm reopenings with longer follow-up and prolonged imaging follow-up has been recommended.8,18 However,

interpretation of these studies is impeded by a wide variety in time intervals of first follow-up angiography. Reopenings that were detected on first follow up angiography some years after coiling, may have had developed much earlier. Recently, studies have found that almost all aneurysm reopenings may occur in the first 6 months after coiling, and that late reopening (>6 months after coiling) is rare.19,20 If indeed, late

aneurysm reopening is rare, and almost all reopened aneurysms can be detected at first imaging follow-up after 6 months, long-term follow-up may not be necessary for a large subgroup of patients.

Another important reason for imaging follow-up of patients with coiled intracranial aneurysms is the detection of newly developed aneurysms or growth of small untreated additional aneurysms. Patients with a treated intracranial aneurysm frequently have additional aneurysms. Incidence of growth of additional aneurysms varies in different studies, with annual risks ranging from 1.51% to 22.7%. The annual risk of developing

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Durability of endovascular treatment for intracranial aneurysms

12

aneurysms are unstable.24 Overall, the annual rupture rate of unruptured intracranial

aneurysms is low, 0.04-1.2% per year.25,26

aims anD outline of this thesis

This thesis is focused on the long-term clinical and angiographic outcome of patients with coiled intracranial aneurysms.

The main objectives of this thesis are:

• To evaluate the yield and psychological effect of MRA screening long term after coiling in patients with adequate aneurysm occlusion at first angiographic follow-up after 6 months

• To systematically review the literature on angiographic outcome and retreatments after coiling of intracranial aneurysms

• To assess long-term clinical and angiographic outcome in patients with incomplete aneurysm occlusion at first angiographic follow-up 6 months after coiling

• To assess long-term clinical and angiographic outcome after endovascular treatment of patients with partially thrombosed intracranial aneurysms

The results of a systematic review and meta-analysis of 42 studies with imaging follow-up of patients with coiled intracranial aneurysms are presented in CHAPTER 2. We evaluated reopening and retreatment rates and risk factors for aneurysm reopening and retreatment.

We performed a multicenter imaging follow-up study with MRA at 3 Tesla >4.5 years after coiling, in 400 patients with 440 adequately occluded aneurysms at first (6-months) angiographic follow-up. In CHAPTER 3 we describe the yield of long-term follow-up screening with MRA in these patients in long-terms of detection of late (>6 months after coiling) aneurysm reopening and indication for retreatment. Additional aneurysms detected 5 years ± 0.5 years after coiling on the long-term follow-up MRA of 276 patients were compared with previous imaging to assess formation of de novo aneurysms and growth of small untreated additional aneurysms. Five-year incidence of de novo aneurysm formation and growth of untreated aneurysms is described in CHAPTER 4. Patients who participated in the LOTUS study (screening with MRA long-term after coiling of an intracranial aneurysm) may experience feelings of anxiety.

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Introduction and outline of the thesis

Chapter 1

13

patient, and thus reduce feelings of anxiety with time. In CHAPTER 5 we studied the effect of screening with MRA on mood and anxiety in 120 participants in the long-term follow-up study after coiling of intracranial aneurysms.

Although the majority of coiled aneurysms is adequately occluded at first angiographic follow-up, a significant part is incompletely occluded. Patients with previously ruptured incompletely occluded aneurysms are at risk of a recurrent SAH. Often, retreatment is performed and imaging follow-up intensified in these patients, exposing them to the risk of procedural complications. In CHAPTER 6 we describe all aneurysm related late adverse events in 124 patients with incompletely occluded aneurysms at first angiographic follow-up 6 months after coiling.

The most consistent risk factor for aneurysm reopening is the presence of intraluminal thrombus in aneurysms. Partially thrombosed intracranial aneurysms are rare and form a high-risk subgroup of intracranial aneurysms. In CHAPTER 7 we assessed long-term clinical and angiographic outcome of 56 patients with endovascular treatment of partially thrombosed aneurysms. Outcomes of two different treatment modalities were investigated; parent vessel occlusion (PVO) and coiling.

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Durability of endovascular treatment for intracranial aneurysms

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references

1. Rinkel GJ, Djibuti M, Algra A, van Gijn J. Prevalence and risk of rupture of intracranial aneurysms: a

systematic review. Stroke 1998;29:251-6

2. Molyneux AJ, Kerr RS, Birks J, Ramzi N, Yarnold J, Sneade M, Rischmiller J, for the ISAT

collaborators. Risk of recurrent subarachnoid hemorrhage, death, or dependence and standardized mortality ratios after clipping or coiling of an intracranial aneurysm in the International

Subarachnoid Aneurysm Trial (ISAT): long-term follow-up. Lancet Neurol 2009;8:427-33.

3. Miller CA, Hill SA, Hunt WE. “De novo” aneurysms- a clinical review. Surg Neurol 1985;24:173-80

4. Wermer MJ, van der Schaaf IC, Algra A, Rinkel GJ. Risk of rupture of unruptured intracranial

aneurysms in relation to patient and aneurysm characteristics: an updated meta-analysis. Stroke 2007;38:1404-10

5. Sluzewski M, van Rooij WJ. Early rebleeding after coiling of ruptured cerebral aneurysms: incidence,

morbidity, and risk factors. AJNR Am J Neuroradiol 2005;26:1739–43

6. Guglielmi G, Viñuela F, Sepetka I, Macellari V. Electrothrombosis of saccular aneurysms via

endovascular approach. Part 1: Electrochemical basis, technique, and experimental results. J Neurosurg 1991;75:1-7

7. Molyneux A, Kerr R, Stratton I, et al. International Subarachnoid Aneurysm Trial (ISAT) of

neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised trial. Lancet 2002;360:1267–74

8. Campi A, Ramzi N, Molyneux AJ, Summers PE, Kerr RS, Sneade M, Yarnold JA, Rischmiller J, Byrne

JV. Retreatment of ruptured cerebral aneurysms in patients randomized by coiling or clipping in the International Subarachnoid Aneurysm Trial (ISAT). Stroke. 2007;38: 1538–1544.

9. Cognard C, Weill A, Spelle L, Piotin M, Castaings L, Rey A, Moret J. Long-term angiographic

follow-up of 169 intracranial berry aneurysms occluded with detachable coils. Radiology. 1999;212:348 –356.

10. Piotin M, Spelle L, Mounayer C, Salles-Rezende MT, Giansante-Abud D, Vanzin-Santos R, Moret J. Intracranial aneurysms: treatment with bare platinum coils—aneurysm packing, complex coils, and angiographic recurrence. Radiology. 2007;243:500 –508.

11. van Rooij WJ, Sprengers ME, Sluzewski M, Beute GN. Intracranial aneurysms that repeatedly reopen over time after coiling: imaging characteristics and treatment outcome. Neuroradiology. 2007;49:343–349.

12. Roy D, Milot G, Raymond J. Endovascular treatment of unruptured aneurysms. Stroke 2001;32:1998-2004

13. Slob MJ, Sluzewski M, van Rooij WJ. The relation between packing and reopening in coiled intracranial aneurysms: a prospective study. Neuroradiology. 2005;47:942–945.

14. Kai Y, Hamada J, Morioka M, Yano S, Kuratsu J. Evaluation of the stability of small ruptured aneurysms with a small neck after embolization with Guglielmi detachable coils: correlation between coil packing ratio and coil compaction. Neurosurgery 2005; 56: 785-92.

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Introduction and outline of the thesis

Chapter 1

15

aneurysms: long-term clinical and serial angiographic results. AJNR Am J Neuroradiol. 2003;24:257–262.

16. Grunwald IQ, Papanagiotou P, Struffert T, Politi M, Krick C, Gu¨l G, Reith W. Recanalization after endovascular treatment of intracerebral aneurysms. Neuroradiology. 2007;49:41– 47.

17. Nguyen TN, Hoh BL, Amin-Hanjani S, Pryor JC, Ogilvy CS. Comparison of ruptured vs unruptured aneurysms in recanalization after coil embolization. Surg Neurol. 2007;68:19 –23.

18. Raymond J, Guilbert F, Weill A, Georganos SA, Juravsky L, Lambert A, Lamoureux J, Chagnon M, Roy D. Long-term angiographic reopenings after selective endovascular treatment of aneurysms with detachable coils. Stroke 2003;34:1398-403.

19. Sluzewski M, van Rooij WJ, Rinkel GJ, Wijnalda D. Endovascular treatment of ruptured intracranial aneurysms with detachable coils: long-term clinical and serial angiographic results. Radiology 2003;227:720–24

20. Gallas S, Januel AC, Pasco A, Drouineau J, Gabrillargues J, Gaston A, Cognard C. Herbreteau D. Long-term follow-up of 1036 cerebral aneurysms treated by bare coils: a multicentric cohort treated between 1998 and 2003. AJNR Am J Neuroradiol 2009;30:1986-92

21. Sprengers ME, van Rooij WJ, Sluzewski M, Rinkel GJE, Velthuis BK, de Kort GAP, Majoie CBLM. MR Angiography follow-up 5 years after coiling: frequency of new aneurysms and enlargement of untreated aneurysms. AJNR Am J Neuroradiol 2009;30:303-07

22. David CA, Vishteh AG, Spetzler RF, Lemole M, Lawton MT, Partovi S. Late angiographic follow-up review of surgically treated aneurysms. J Neurosurg 1999;91:396–401

23. Wermer MJ, van der Schaaf IC, Velthuis BK, Algra A, Buskens E, Rinkel GJ, for the ASTRA Study Group. Follow-up screening after subarachnoid haemorrhage: frequency and determinants of new aneurysms and enlargement of existing aneurysms. Brain 2005;128:2421–29.

24. Wiebers DO, Whisnant JP, Huston J III, Meissner I, Brown RD Jr, Piepgras DG, Forbes GS, Thielen K, Nichols D, O’Fallon WM, Peacock J, Jaeger L, Kassel NF, Kongable-Beckman GL, Torner JC; International Study of Unruptured Intracranial Aneurysms Investigators. Unruptured intracranial aneurysms: natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet 2003;362:103-10

25. Molyneux AJ, Kerr RS, Birks J, Ramzi N, Yarnold J, Sneade M, Rischmiller J, for the ISAT collaborators. Risk of recurrent subarachnoid hemorrhage, death, or dependence and standardized mortality ratios after clipping or coiling of an intracranial aneurysm in the International

Subarachnoid Aneurysm Trial (ISAT): long-term follow-up. Lancet Neurol 2009;8:427-33. 26. Wermer MJ, van der Schaaf IC, Algra A, Rinkel GJ. Risk of rupture of unruptured intracranial

aneurysms in relation to patient and aneurysm characteristics: an updated meta-analysis. Stroke 2007;38:1404-10

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Durability of endovascular treatment for intracranial aneurysms

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2

Coiling of intracranial

aneurysms

A systematic review on initial

occlusion and reopening and

retreatment rates

S.P. Ferns M.E.S. Sprengers W.J.J. van Rooij G.J.E. Rinkel J.C. van Rijn S. Bipat M. Sluzewski C.B.L.M. Majoie

2

Coiling of intracranial

aneurysms

A systematic review on initial

occlusion and reopening and

retreatment rates

S.P. Ferns M.E.S. Sprengers W.J.J. van Rooij G.J.E. Rinkel J.C. van Rijn S. Bipat M. Sluzewski C.B.L.M. Majoie

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Chapter 2 Coiling of intracranial aneurysms

19

abstract

background and purpose

The proportion of incompletely occluded aneurysms after coiling varies widely between studies. To assess overall outcome of coiling, we systematically reviewed the literature to determine initial occlusion, reopening, and retreatment rates of coiled aneurysms according to predefined criteria and subgroups.

methods

We searched PubMed and EMBASE (January 1999 to September 2008) for studies of >50 coiled aneurysms. Two reviewers independently extracted data. We grouped studies reporting on only ruptured aneurysms, posterior circulation aneurysms, and studies with large proportions of aneurysms >10 mm to assess possible determinants for incomplete occlusion, reopening, and retreatment.

results

Forty-six studies totaling 8161 coiled aneurysms met inclusion criteria. Immediately after coiling, 91.2% (95%CI, 90.6%- 91.9%) of the aneurysms were adequately occluded. Aneurysm reopening occurred in 20.8% (95% CI, 19.8%- 21.9%) and retreatment was performed in 10.3% (95% CI, 9.5- 11.0%). Reopening rate was lower in studies reporting on ruptured aneurysms only compared with all studies (11.4% versus 20.8%; relative risk, 0.55; 95% CI, 0.47- 0.64) and higher in studies focusing on posterior circulation aneurysms compared with studies with >85% anterior circulation aneurysms (22.5% versus 15.5%; relative risk, 1.5; 95% CI, 1.2- 1.7). Regression analysis showed higher retreatment rates with increasing proportion of aneurysms >10 mm (β= 0.252; 95% CI, 0.073- 0.432). We could not find a relation between reopening and type of coils used.

conclusions

At follow-up, one fifth of all coiled intracranial aneurysms shows reopening of which half is retreated. Possible risk factors for aneurysm reopening are location in the posterior circulation and size >10 mm. To confirm our findings, a meta-analysis on individual well-reported patient data is desirable.

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Durability of endovascular treatment for intracranial aneurysms

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introDuction

Endovascular treatment with coils has become an established treatment modality for both ruptured and unruptured intracranial aneurysms.1,2 Coiling has several

shortcomings. Not all aneurysms can be occluded completely at first treatment, leaving the patient at risk for early recurrent hemorrhage in case of a recently ruptured aneurysm.1 Another drawback is the possibility of reopening of an initially adequately occluded aneurysm with time.3–13

Possible determinants for initial incomplete aneurysm occlusion are unfavorable aneurysm anatomy and vessel geometry and types of coils that are used. Possible risk factors for reopening of a coiled aneurysm over time are large aneurysm size,7,14,15

presence of intraluminal thrombus,12 low packing density,11,16 initial incomplete

occlusion,17,18 duration of follow-up,6,7 ruptured aneurysms,19 location in the posterior

circulation,3 and a large neck–dome ratio.20,21 The actual influence of risk factors for

incomplete occlusion and reopening remains obscure. As a consequence, the yield and implication of long-term imaging follow-up is largely unclear and an optimal follow-up protocol for individual patients is hard to define.

The purpose of this systematic review of the literature was to assess the overall proportion of coiled aneurysms that is incompletely occluded at initial treatment, the proportion of aneurysms that reopens over time, and the proportion of aneurysms that is retreated. In addition, we aimed to assess whether rupture status, location in posterior or anterior circulation, use of standard or modified coils, aneurysm size, and duration of follow-up influenced the occurrence of these events.

methoDs

literature search

We searched PubMed and EMBASE from January 1999 through September 2008. The following key words as MESH terms and text words were used in relevant combinations: “subarachnoid hemorrhage,” “intracranial aneurysm,” “endovascular treatment,” and “coiling” in both “AND” and “OR” combinations. The search was restricted to human studies in English, German, Spanish, and French. To assess eligibility, 2 reviewers (M.E.S.S. and S.P.F.) independently checked all abstracts and retrieved full-text articles on inclusion criteria using a standardized data extraction form.

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Chapter 2 Coiling of intracranial aneurysms

21

eligibility

We included studies of >50 patients and imaging follow-up with angiography or MR angiography. Studies using standard coils and modified coils (polyglycolic acid-coated coils such as Matrix [Boston Scientific, Freemont, Calif], Nexus [EV3, Irvine, Calif], Cerecyte [Micrus Endovascular, San Jose, Calif], and Hydrocoils [MicroVention, Aliso Viejo, Calif]) were considered for inclusion. Studies that included traumatic, dissecting, mycotic, and flow-related aneurysms and studies that included parent vessel coil occlusions and retreatments after previous coilings were only considered eligible when these aneurysms and treatments could be separated from the entire cohort. Initial treatment results and duration and results of follow-up imaging had to be clearly described.

selection of studies and data extraction

From the studies that met the inclusion criteria, 2 reviewers (M.E.S.S. and S.P.F.) independently extracted relevant data. Demographics included number of patients, gender, age, number and location of included aneurysms, number of ruptured and unruptured aneurysms, and aneurysm size. We extracted mean size of the aneurysms and, if possible, we dichotomized sizes in ≤10 mm and >10 mm. Data extracted for the coil procedure included type of coils used and initial aneurysm occlusion status. Occlusion status initially and at follow-up was classified as complete (100%, total), near complete (neck remnant, dog-ear, 90% to 98%), or incomplete (aneurysm remnant, residual aneurysm filling, <90%). The term “adequate occlusion” was used for completely and near completely occluded aneurysms. Subsequently, aneurysm occlusion status was categorized on a 2-point scale (adequate versus incomplete occlusion) and a 3-point scale (complete, near complete, and incomplete occlusion). Follow-up data included mean, median, and range of follow-up duration and number of patients with follow-up. We interpreted terms as “aneurysm recurrence,” “new filling of aneurysm lumen,” “recanalization,” and “regrowth” as reopening of the aneurysm. Numbers of retreatments were recorded. If data were presented graphically or as percentages, crude numbers were deducted or calculated. When the same patient population was the subject of several publications, only the study with the largest sample size was included.

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Durability of endovascular treatment for intracranial aneurysms

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Data analysis

Cumulative data on initial aneurysm occlusion and occlusion at follow-up, reopening, and retreatment were calculated as proportions with corresponding 95% confidence intervals (CI). We multiplied the number of aneurysms by the average duration of follow-up to obtain the total number of aneurysm years of follow-up. To assess whether location in posterior circulation, rupture status, and type of coil that was used were risk factors for initial incomplete occlusion, reopening, and retreatment, we determined occurrence of these events in studies reporting on these data. We used the χ2 test to assess differences for all outcomes and we calculated relative risks (RR) with corresponding 95% CIs of risk factors for reopening and retreatment alone.

The influence of aneurysm size >10 mm on the risk of reopening and retreatment was assessed with linear regression analysis with proportion of aneurysms >10 mm as the independent variable and reopening and retreatment rates as outcomes. The lack of fixed follow-up duration in most studies precluded analysis of the correlation between increasing duration of follow-up and reopening and retreatment rate.

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Chapter 2 Coiling of intracranial aneurysms

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results

search results

The initial search in PubMed and EMBASE yielded 2830 articles (Figure 1). Of all articles 2749 were excluded based on review of titles and abstracts. The most frequent reasons for exclusion were lack of imaging follow-up and sample size <50 patients. Of the 81 full-text publications, 35 were excluded; 19 studies did not clearly describe follow-up duration, 5 studies did not report initial occlusion results, 5 studies did not separately report a subgroup treated with parent artery occlusion, 4 studies had included retreated aneurysms in the final aneurysm occlusion rates, and 3 studies were excluded because of double publication of the same sample.22–24 Finally, 46 studies

were included. Four of the 46 studies compared 2 groups of aneurysms with separately reported patient and aneurysms characteristics and follow-up results.25–28

All included 46 studies are available in the supplemental appendix.

baseline characteristics

Baseline characteristics of the 46 studies that reported on 8161 coiled aneurysms are displayed in Table 1. In 42 studies with 7865 aneurysms, 5141 (65.4%) aneurysms were ruptured and 2724 (34.6%) aneurysms were unruptured. Of all 8161 aneurysms, 6241 (76.5%) had imaging follow-up for a total of 8328 aneurysm years. Mean duration of follow-up ranged from 4.6 to 38 months with an average of the mean of 14.1 months. Most studies lacked fixed follow-up intervals.

In 37 studies with 6968 aneurysms, 4640 aneurysms were located in the anterior circulation (66.7%) and 2328 (33.3%) in the posterior circulation. In 20 studies with 3288 aneurysms, mean aneurysm size ranged from 5 to 11 mm with an average of the mean of 7 mm. In 29 studies with 5302 aneurysms, 1239 (23.4%) were >10 mm.

In 31 studies with 6226 aneurysms, treatment was performed with standard bare platinum coils. In 6 studies with 482 aneurysms, treatment was performed with modified coils.

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Durability of endovascular treatment for intracranial aneurysms

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treatment results

Initial aneurysm occlusion

Initial aneurysm occlusion status was reported in 37 studies with 6991 aneurysms on a 3-point scale. Complete initial occlusion was reported in 4355 aneurysms (62.3%; 95% CI, 61.2- 63.4%), near complete occlusion in 2065 aneurysms (29.5%; 95% CI, 28.5- 30.6%), and incomplete occlusion in 571 aneurysms (8.2%; 95% CI, 7.5- 8.8%; Table 2). Converting these results into a 2-point scale and adding the results of 9 studies with 1049 aneurysms that reported on a 2-point scale resulted in all 46 studies with 8040 aneurysms (121 aneurysms were excluded due to incomplete reporting of occlusion results in 2 studies). Initial aneurysm occlusion was adequate in 7335 aneurysms (91.2%; 95% CI, 90.6- 91.9%) and incomplete in 705 aneurysms (8.8%; 95% CI, 8.2- 9.4%).

Aneurysm occlusion at follow-up

Aneurysm occlusion at follow-up was reported in 19 studies with 2882 aneurysms on a 3-point scale. Occlusion was complete in 1772 aneurysms (61.5%; 95% CI, 59.7- 63.3%), near complete in 654 aneurysms (22.7%; 95% CI, 21.2- 24.2%), and incomplete in 456 aneurysms (15.8%; 95% CI, 14.5- 17.2%). Converting these results into a 2-point scale and adding the results of 8 studies with 777 aneurysms that reported on a 2-point scale resulted in 27 studies with 3659 aneurysms. Adequate aneurysm occlusion was reported in 3054 aneurysms (83.4%; 95% CI, 82.3- 84.7%) and incomplete occlusion in 605 aneurysms (16.6%; 95% CI, 15.3- 17.7%; Table 2).

Reopening and retreatment rates

Reopening rate was reported in 42 studies with 5926 aneurysms. Retreatment rates were reported in 41 studies with 5582 aneurysms (Table 2). At a mean follow-up ranging from 4.7 to 38 months (Figure 2), 1235 of 5926 aneurysms reopened and 572 of 5582 aneurysms were retreated. Reopening rate was 20.8% (95% CI, 19.8- 21.9%) and retreatment rate was 10.3% (95% CI, 9.5%- 11.0%).

Ruptured aneurysms

Nine studies with 1786 aneurysms reported on ruptured aneurysms only. These studies had significantly higher proportions of initially and at follow-up adequately occluded aneurysms (95.9% versus 91.2% and 90.3% versus 83.4%) and lower reopening

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Durability of endovascular treatment for intracranial aneurysms

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all studies. Relative risk for reopening of aneurysms in studies with only ruptured aneurysms was 0.55 (95% CI, 0.47- 0.64) and for retreatment 0.70 (95% CI, 0.37- 0.86) compared with studies including ruptured as well as unruptured aneurysms (Table 2).

Posterior versus anterior circulation aneurysms

Six studies that reported on 862 aneurysms located in the posterior circulation only were compared with 8 studies reporting on 1901 aneurysms with >85% of aneurysms located in the anterior circulation. There was no difference in proportion adequate initial occlusion (91.6% versus 92.1%), but the proportion of posterior circulation aneurysms adequately occluded at follow-up was lower (70.4% versus 92.6%), and reopening and retreatment rates were higher (22.5% versus 15.5% and 14.5% versus 6.5%) compared with studies with >85% anterior circulation aneurysms. Relative risk for reopening of studies reporting on posterior circulation aneurysms was 1.45 (95% CI, 1.23- 1.72) and for retreatment 2.22 (95% CI, 1.73- 2.86) compared with studies including >85% anterior circulation aneurysms (Table 2).

Standard platinum coils versus modified coils

Proportion of aneurysms with initial adequate occlusion was significantly lower for aneurysms treated with modified coils compared with aneurysms treated with standard platinum coils (88.8% versus 92.1%; relative risk, 0.96; 95% CI, 0.93- 0.996). At follow-up, the proportion of aneurysms with adequate occlusion was not different (85.9% versus 86.8%) and reopening and retreatment rates were not different (21.6% versus 20.1% and 11.7% versus 9.6%; Table 2).

Aneurysm size >10 mm

In 29 studies, the proportion of aneurysms >10 mm was reported; there were no studies with exclusively small or only large aneurysms. Of these 29 studies, 27 reported reopening rate and 24 reported retreatment rate. We created a scatter plot with reopening rate and retreatment rate as dependent variables and proportion aneurysms >10 mm as the independent variable (Figure 3). Regression analysis showed increasing reopening rates with increasing proportions of aneurysms >10 mm (β= 0.124; 95% CI, -0.165- 0.414) and increasing retreatment rate in studies with increasing proportions of aneurysms >10 mm (β= 0.252; 95% CI, 0.073- 0.432). The β indicates that for 1% more aneurysms >10 mm, reopening increases with 0.12% and retreatment increases with 0.25%.

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Chapter 2 Coiling of intracranial aneurysms

29

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Durability of endovascular treatment for intracranial aneurysms

30

figure 3. Regression analysis: reopening and retreatment rates in studies with increasing proportions of

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Chapter 2 Coiling of intracranial aneurysms

31

Discussion

Our review of >8000 coiled intracranial aneurysms shows that 91% of aneurysms were adequately occluded at initial treatment. At follow-up of various intervals, 83% of treated aneurysms were adequately occluded. Reopening occurred in 21% of aneurysms and 10% of aneurysms were retreated. The difference between proportion of aneurysms with reopening (21%) and proportion of aneurysms with retreatment (10%) indicates that not all reopenings were retreated. Some reopened aneurysms may not be judged suitable for retreatment because of unfavorable geometry, small size, or high anticipated risk of retreatment.

Studies with exclusively ruptured aneurysms had higher adequate occlusion rates both initially and at follow-up compared with all studies and lower reopening and retreatment rates. Although several studies state that rupture of the aneurysm is a risk factor for reopening of coiled aneurysms,7,19 our review could not confirm this finding.

It is likely that higher proportions of large and posterior localization in unruptured aneurysms explain the higher rate of reopening of unruptured aneurysms.29 Because

we had no data on individual patients or individual aneurysms but only aggregated data per study population, we could not assess whether indeed these factors explain the observed difference in reopening between ruptured and unruptured aneurysms.

Studies with exclusively posterior circulation aneurysms had higher proportions of incompletely occluded aneurysms at follow-up with higher proportions of reopening and retreatment compared with the studies with >85% anterior circulation aneurysms. This is in concordance with previous studies.3,15,30 A possible explanation is that surgery

is less likely an option in posterior circulation aneurysms. This could imply that also posterior circulation aneurysms with unfavorable configuration are coiled, whereas aneurysms with unfavorable configuration in the anterior circulation are clipped.

Studies with aneurysms treated with modified coils did not show higher occlusion rates compared with studies using standard platinum coils. In fact, initial occlusion rates were less favorable. At follow-up, reopening and retreatment rates were comparable to standard platinum coils. This is consistent with a recent review regarding this subject.31 The lower rate of initial occlusion with modified coils may be

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Durability of endovascular treatment for intracranial aneurysms

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different kinds of modified coils were grouped together and that results might thus not apply to specific types of coils.

A higher retreatment rate was found in studies with increasing proportion of aneurysms >10 mm. Large aneurysm size is a well-established risk-factor for reopening and retreatment, in part explained by lesser packing density and a higher proportion of aneurysms with intraluminal thrombus.7,11,14,15 We could not assess an association of

increased reopening and retreatment rates with longer duration of follow-up, because fixed follow-up intervals were lacking. An analysis with mean duration of follow-up would not be meaningful. Although we did put all studies that reported reopening and their available follow-up duration into a forest plot, this also shows that there is no association or even trend in reopening and increasing follow-up duration (figure 2).

This study had several limitations. Although our search was extensive, there is a chance that some studies were not included. The available literature is limited by a lack of randomized studies, lack of standard definitions, lack of fixed follow-up intervals, absence of details of individual patients, and no description of selection of patients. Reporting quality in most studies was poor allowing aggravated data extraction only. In addition, data were not reported in a standardized way and follow-up intervals varied widely. Reopening, retreatment, or recurrent hemorrhage could not be ascribed to individual patients or aneurysms, making it difficult to statistically assess possible risk factors for these events. A recent study provides future authors with detailed reporting standards of endovascular repair of saccular intracranial cerebral aneurysms.32

conclusions

With this review, we have given an overview of the literature concerning aneurysm occlusion, reopening, and retreatment. To asses the value of long-term imaging follow-up, the timing of occurrence of reopening should be known and studies with fixed follow-up intervals are needed. Future research should be focused on patients and aneurysms with specific risk factors for reopening and recurrent hemorrhage. With this information, customized follow-up protocols can be designed resulting in better patient care and reduced costs.

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Chapter 2 Coiling of intracranial aneurysms

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references

1. Molyneux AJ, Kerr RS, Yu LM, Clarke M, Sneade M, Yarnold JA, Sandercock P. International

Subarachnoid Aneurysm Trial (ISAT) Collaborative Group. International Subarachnoid Aneurysm Trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: a randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet. 2005;366:809–817.

2. Brilstra EH, Rinkel GJ, van der Graaf Y, van Rooij WJ, Algra A. Treatment of intracranial aneurysms

by embolization with coils: a systematic review. Stroke. 1999;30:470–476.

3. Campi A, Ramzi N, Molyneux AJ, Summers PE, Kerr RS, Sneade M, Yarnold JA, Rischmiller J, Byrne

JV. Retreatment of ruptured cerebral aneurysms in patients randomized by coiling or clipping in the International Subarachnoid Aneurysm Trial (ISAT). Stroke. 2007;38: 1538–1544.

4. Cognard C, Weill A, Spelle L, Piotin M, Castaings L, Rey A, Moret J. Long-term angiographic

follow-up of 169 intracranial berry aneurysms occluded with detachable coils. Radiology. 1999;212:348–356.

5. Henkes H, Fischer S, Liebig T, Weber W, Reinartz J, Miloslavski E, Kühne D. Repeated endovascular

coil occlusion in 350 of 2759 intracranial aneurysms: safety and effectiveness aspects. Neurosurgery. 2008;62:1532–1537.

6. Piotin M, Spelle L, Mounayer C, Salles-Rezende MT, Giansante-Abud D, Vanzin-Santos R, Moret J.

Intracranial aneurysms: treatment with bare platinum coils—aneurysm packing, complex coils, and angiographic recurrence. Radiology. 2007;243:500–508.

7. Raymond J, Guilbert F, Weill A, Georganos SA, Juravsky L, Lambert A, Lamoureux J, Chagnon M,

Roy D. Long-term angiographic recurrences after selective endovascular treatment of aneurysms with detachable coils. Stroke. 2003;34:1398 –1403.

8. Slob MJ, Sluzewski M, van Rooij WJ. The relation between packing and reopening in coiled

intracranial aneurysms: a prospective study. Neuroradiology. 2005;47:942–945.

9. Sluzewski M, van Rooij WJ, Rinkel GJ, Wijnalda D. Endovascular treatment of ruptured intracranial

aneurysms with detachable coils: long-term clinical and serial angiographic results. Radiology. 2003;227:720–724.

10. Sluzewski M, Menovsky T, van Rooij WJ, Wijnalda D. Coiling of very large or giant cerebral aneurysms: long-term clinical and serial angiographic results. AJNR Am J Neuroradiol. 2003;24:257–262.

11. Sluzewski M, van Rooij WJ, Slob MJ, Bescós JO, Slump CH, Wijnalda D. Relation between aneurysm volume, packing, and compaction in 145 cerebral aneurysms treated with coils. Radiology. 2004;231:653– 658.

12. van Rooij WJ, Sprengers ME, Sluzewski M, Beute GN. Intracranial aneurysms that repeatedly reopen over time after coiling: imaging characteristics and treatment outcome. Neuroradiology. 2007;49:343–349.

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14. Vallee JN, Aymard A, Vicaut E, Reis M, Merland JJ. Endovascular treatment of basilar tip aneurysms with Guglielmi detachable coils: predictors of immediate and long-term results with multivariate analysis 6-year experience. Radiology. 2003;226:867– 879.

15. Peluso JP, van Rooij WJ, Sluzewski M, Beute GN. Coiling of basilar tip aneurysms: results in 154 consecutive patients with emphasis on recurrent haemorrhage and re-treatment during mid- and long-term follow-up. J Neurol Neurosurg Psychiatry. 2008;79:706 –711.

16. Kawanabe Y, Sadato A, Taki W, Hashimoto N. Endovascular occlusion of intracranial aneurysms with Guglielmi detachable coils: correlation between coil packing density and coil compaction. Acta Neurochir (Wien). 2001;143:451–455.

17. Li MH, Gao BL, Fang C, Gu BX, Cheng YS, Wang W, Scotti G. Angiographic follow-up of cerebral aneurysms treated with Guglielmi detachable coils: an analysis of 162 cases with 173 aneurysms. AJNR Am J Neuroradiol. 2006;27:1107–1112.

18. Grunwald IQ, Papanagiotou P, Struffert T, Politi M, Krick C, Gül G, Reith W. Recanalization after endovascular treatment of intracerebral aneurysms. Neuroradiology. 2007;49:41– 47.

19. Nguyen TN, Hoh BL, Amin-Hanjani S, Pryor JC, Ogilvy CS. Comparison of ruptured vs unruptured aneurysms in recanalization after coil embolization. Surg Neurol. 2007;68:19–23.

20. Ries T, Siemonsen S, Thomalla G, Grzyska U, Zeumer H, Fiehler J. Long-term follow-up of cerebral aneurysms after endovascular therapy prediction and outcome of retreatment. AJNR Am J Neuroradiol. 2007;28:1755–1761.

21. Kai Y, Hamada J, Morioka M, Yano S, Kuratsu J. Evaluation of the stability of small ruptured aneurysms with a small neck after embolization with Guglielmi detachable coils: correlation between coil packing ratio and coil compaction. Neurosurgery. 2005;56:785–792.

22. Murayama Y, Viñuela F, Duckwiler, GR Gobin YP, Guglielmi G. Embolization of incidental cerebral aneurysms by using the Guglielmi detachable coil system. J Neurosurg. 1999;90:207–214.

23. Tateshima S, Murayama Y, Gobin YP, Duckwiler GR, Guglielmi G, Viñuela F. Endovascular treatment of basilar tip aneurysms using Guglielmi detachable coils: anatomic and clinical outcomes in 73 patients from a single institution. Neurosurgery. 2000;47:1332–1339.

24. Roy D, Milot G, Raymond J. Endovascular treatment of unruptured aneurysms. Stroke. 2001;32:1998 –2004.

25. Kang HS, Han MH, Kwon BJ, Jung C. Short-term outcome of intracranial aneurysms treated with polyglycolic acid/lactide copolymer-coated coils compared to historical controls treated with bare platinum coils: a singlecenter experience. AJNR Am J Neuroradiol. 2005;26:1921–1928. 26. Slob MJ, van Rooij WJ, Sluzewski M. Influence of coil thickness on packing, re-opening and

retreatment of intracranial aneurysms: a comparative study between two types of coils. Neurol Res. 2005;27(suppl 1):S116–S119.

27. Gaba RC, Ansari SA, Roy SS, Marden FA, Viana MA, Malisch TW. Embolization of intracranial aneurysms with hydrogel-coated coils versus inert platinum coils: effects on packing density, coil length and quantity, procedure performance, cost, length of hospital stay, and durability of therapy. Stroke. 2006;37:1443–1450.

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Chapter 2 Coiling of intracranial aneurysms

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28. Bendszus M, Bartsch AJ, Solymosi L. Endovascular occlusion of aneurysms using a new bioactive

coil: a matched pair analysis with bare platinum coils. Stroke. 2007;38:2855–2857.

29. Unruptured intracranial aneurysms—risk of rupture and risks of surgical intervention. International Study of Unruptured Intracranial Aneurysms Investigators. N Engl J Med. 1998;339:1725–1733. 30. Henkes H, Fischer S, Mariushi W, Weber W, Liebig T, Miloslavski E, Brew S, Kühne D. Angiographic

and clinical results in 316 coil-treated basilar artery bifurcation aneurysms. J Neurosurg. 2005;103:990 –999.

31. Kurre W, Berkefeld J. Materials and techniques for coiling of cerebral aneurysms: how much scientific evidence do we have? Neuroradiology. 2008;50:909 –927.

32. Meyers PM, Schumacher HC, Higashida RT, Derdeyn CP, Nesbit GM, Sacks D, Wechsler LR, Bederson JB, Lavine SD, Rasmussen P. Reporting standards for endovascular repair of saccular intracranial cerebral aneurysms. Stroke. 2009;40:e366.

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appendix 1. reference list of included studies for review

1. Byrne JV, Sohn MJ, Molyneux AJ, Chir B. Five-year experience in using coil embolization for

ruptured intracranial aneurysms: outcomes and incidence of late rebleeding. J Neurosurg 1999; 90: 656-63.

2. Lempert TE, Malek AM, Halbach VV Phatouros CC, Meyers PM, Dowd CF, Higashida RT.

Endovascular treatment of ruptured posterior circulation cerebral aneurysms. Clinical and angiographic outcomes. Stroke 2000; 31: 100-10.

3. Bracard S, Lebedinsky A, Anxionnat R, Neto JM, Audibert G, Long Y, Picard L. Endovascular

treatment of Hunt and Hess grade IV and V aneurysms. AJNR Am J Neuroradiol 2002; 23: 953-57.

4. Tamatani S, Ito Y, Abe H, Koike T, Takeuchi S, Tanaka R. Evaluation of the stability of aneurysms

after embolization using detachable coils: correlation between stability of aneurysms and embolized volume of aneurysms. AJNR Am J Neuroradiol 2002; 23: 762-7.

5. Thornton J, Debrun GM, Aletich VA, Bashir Q, Charbel FT, Ausman J. Follow-up angiography

of intracranial aneurysms treated with endovascular placement of Guglielmi detachable coils. Neurosurgery 2002; 50: 239-49.

6. Groden C, Eckert B, Ries T, Probst EN, Kucinski T, Zeumer H. Angiographic follow-up of

vertebrobasilar artery aneurysms treated with detachable coils. Neuroradiology 2003; 45: 435-40.

7. Murayama Y, Nien YL, Duckwiler G, Gobin YP, Jahan R, Frazee J, Martin N, Viñuela F. Guglielmi

detachable coil embolization of cerebral aneurysms: 11 years’ experience. J Neurosurg 2003; 98: 959-66.

8. Raymond J, Guilbert F, Weill A, Georganos SA, Juravsky L, Lambert A, Lamoureux J, Chagnon M,

Roy D. Long-term angiographic recurrences after selective endovascular treatment of aneurysms with detachable coils. Stroke 2003; 34: 1398-403.

9. Sluzewski M, van Rooij WJ, Rinkel GJ, Wijnalda D. Endovascular treatment of ruptured intracranial

aneurysms with detachable coils: long-term clinical and serial angiographic results. Radiology 2003; 227: 720-4.

10. Vallee JN, Aymard A, Vicaut E, Reis M, Merland JJ. Endovascular treatment of basilar tip aneurysms with Guglielmi detachable coils: predictors of immediate and long-term results with multivariate analysis 6-year experience. Radiology 2003; 226: 867-79.

11. Yu SC, Chan MS, Boet R, Wong JK, Lam JM, Poon WS. Intracranial aneurysms treated with Guglielmi detachable coils: midterm clinical and radiological outcome in 97 consecutive Chinese patients in Hong Kong. AJNR Am J Neuroradiol 2004; 25: 307-13.

12. Fiorella D, Albuquerque FC, Deshmukh VR, McDougall CG. Usefulness of the Neuroform stent for the treatment of cerebral aneurysms: results at initial (3-6-mo) follow-up. Neurosurgery 2005; 56: 1191-201.

13. Gallas S, Pasco A, Cottier JP, Gabrillargues J, Drouineau J, Cognard C, Herbreteau D. A multicenter study of 705 ruptured intracranial aneurysms treated with Guglielmi detachable coils. AJNR Am J Neuroradiol 2005; 26: 1723-31.

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Chapter 2 Coiling of intracranial aneurysms

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14. Henkes H, Fischer S, Mariushi W, Weber W, Liebig T, Miloslavski E, Brew S, Kühne D. Angiographic

and clinical results in 316 coil-treated basilar artery bifurcation aneurysms. J Neurosurg 2005; 103: 990-9.

15. Iijima A, Piotin M, Mounayer C, Spelle L, Weill A, Moret J. Endovascular treatment with coils of 149 middle cerebral artery berry aneurysms. Radiology 2005; 237: 611-9.

16. Kai Y, Hamada J, Morioka M, Yano S, Kuratsu J. Evaluation of the stability of small ruptured aneurysms with a small neck after embolization with Guglielmi detachable coils: correlation between coil packing ratio and coil compaction. Neurosurgery 2005; 56: 785-92.

17. Kang HS, Han MH, Kwon BJ, Kwon OK, Kim SH, Choi SH, Chang KH. Short-term outcome of intracranial aneurysms treated with polyglycolic acid/lactide copolymer-coated coils compared to historical controls treated with bare platinum coils: a single-center experience. AJNR Am J Neuroradiol 2005; 26: 1921-8.

18. Linfante I, Akkawi NM, Perlow A, Andreone V, Wakhloo AK. Polyglycolide/polylactide-coated platinum coils for patients with ruptured and unruptured cerebral aneurysms: a single-center experience. Stroke 2005; 36: 1948-53.

19. Murphy M, Bell D, Worth RD, Jehle KS, Critchley GR, Norris JS. Angiography postclipping and coiling of cerebral aneurysms. Br J Neurosurg 2005; 19: 225-8.

20. Slob MJ, van Rooij WJ, Sluzewski M. Influence of coil thickness on packing, re-opening and retreatment of intracranial aneurysms: a comparative study between two types of coils. Neurol Res 2005; 27 Suppl 1: S116-S119.

21. Yagi K, Satoh K, Satomi, Matsubara S, Nagahiro S. Evaluation of aneurysm stability after endovascular embolization with Guglielmi detachable coils: correlation between long-term stability and volume embolization ratio. Neurol Med Chir (Tokyo) 2005; 45: 561-5.

22. Fiorella D, Albuquerque FC, McDougall CG. Durability of aneurysm embolization with matrix detachable coils. Neurosurgery 2006; 58: 51-9.

23. Gaba RC, Ansari SA, Roy SS, Marden FA, Viana MA, Malisch TW. Embolization of intracranial aneurysms with hydrogel-coated coils versus inert platinum coils: effects on packing density, coil length and quantity, procedure performance, cost, length of hospital stay, and durability of therapy. Stroke 2006; 37: 1443-50.

24. Gauvrit JY, Leclerc X, Caron S, Taschner CA, Lejeune JP, Pruvo JP. Intracranial aneurysms treated with Guglielmi detachable coils: imaging follow-up with contrast-enhanced MR angiography. Stroke 2006; 37: 1033-7.

25. Li MH, Gao BL, Fang C, Gu BX, Cheng YS, Wang W, Scotti G. Angiographic follow-up of cerebral aneurysms treated with Guglielmi detachable coils: an analysis of 162 cases with 173 aneurysms. AJNR Am J Neuroradiol 2006; 27: 1107-12.

26. Murayama Y, Vinuela F, Ishii A, Nien YL, Yuki I, Duckwiler G, Jahan R. Initial clinical experience with matrix detachable coils for the treatment of intracranial aneurysms. J Neurosurg 2006; 105:

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Durability of endovascular treatment for intracranial aneurysms

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27. Suzuki S, Jahan R, Duckwiler GR, Frazee J, Martin N, Viñuela F. Contribution of endovascular therapy to the management of poor-grade aneurysmal subarachnoid hemorrhage: Clinical and angiographic outcomes. J Neurosurg 2006; 105: 664-70.

28. Bendszus M, Bartsch AJ, Solymosi L. Endovascular occlusion of aneurysms using a new bioactive coil: a matched pair analysis with bare platinum coils. Stroke 2007; 38: 2855-7.

29. Grunwald IQ, Papanagiotou P, Struffert T, Politi M, Krick C, Gül G, Reith W.. Recanalization after endovascular treatment of intracerebral aneurysms. Neuroradiology 2007; 49: 41-7.

30. Hirsch JA, Bendok BR, Paulsen RD, Cognard C, Campos J, Cronqvist M.. Midterm Clinical Experience with a Complex-shaped Detachable Platinum Coil System for the Treatment of Cerebral Aneurysms: Trufill DCS Orbit Detachable Coil System Registry Interim Results. J Vasc Interv Radiol 2007; 18: 1487-94.

31. Mitra D, Herwadkar A, Soh C, Gholkar A. Follow-up of intracranial aneurysms treated with matrix detachable coils: a single-center experience. AJNR Am J Neuroradiol 2007; 28: 362-7.

32. Nguyen TN, Hoh BL, min-Hanjani S, Pryor JC, Ogilvy CS. Comparison of ruptured vs unruptured aneurysms in recanalization after coil embolization. Surg Neurol 2007; 68: 19-23.

33. Pandey AS, Koebbe C, Rosenwasser R, Veznedaroglu E. Endovascular coil embolization of ruptured and unruptured posterior circulation aneurysms: review of a 10-year experience. Neurosurgery 2007; 60: 626-36.

34. Piotin M, Spelle L, Mounayer , Salles-Rezende MT, Giansante-Abud D, Vanzin-Santos R, Moret J. Intracranial aneurysms: treatment with bare platinum coils--aneurysm packing, complex coils, and angiographic recurrence. Radiology 2007; 243: 500-8.

35. Ries T, Siemonsen S, Thomalla G, Grzyska U, Zeumer H, Fiehler J. Long-term follow-up of cerebral aneurysms after endovascular therapy prediction and outcome of retreatment. AJNR Am J Neuroradiol 2007; 28: 1755-61.

36. Wakhloo AK, Gounis MJ, Sandhu JS, Akkawi N, Schenck AE, Linfante I. Complex-shaped platinum coils for brain aneurysms: higher packing density, improved biomechanical stability, and midterm angiographic outcome. AJNR Am J Neuroradiol 2007; 28: 1395-400.

37. Butteriss D, Gholkar A, Mitra D, Birchall D, Jayakrishnan V. Single-center experience of cerecyte coils in the treatment of intracranial aneurysms: initial experience and early follow-up results. AJNR Am J Neuroradiol 2008; 29: 53-6.

38. Gallas S, Drouineau J, Gabrillargues J, Pasco A, Cognard C, Pierot L, Herbreteau D. Feasibility, procedural morbidity and mortality, and long-term follow-up of endovascular treatment of 321 unruptured aneurysms. AJNR Am J Neuroradiol 2008; 29: 63-8.

39. Geyik S, Yavuz K, Ergun O, Koc O, Cekirge S, Saatci I. Endovascular treatment of intracranial aneurysms with bioactive Cerecyte coils: effects on treatment stability. Neuroradiology 2008; 50: 787-93.

40. Natarajan SK, Sekhar LN, Ghodke B, Britz GW, Bhagawati D, Temkin N. Outcomes of ruptured intracranial aneurysms treated by microsurgical clipping and endovascular coiling in a high-volume center. AJNR Am J Neuroradiol 2008; 29: 753-9.

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Chapter 2 Coiling of intracranial aneurysms

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41. Peluso JP, van Rooij WJ, Sluzewski M, Beute GN. Coiling of basilar tip aneurysms: results in 154

consecutive patients with emphasis on recurrent haemorrhage and re-treatment during mid- and long-term follow-up. J Neurol Neurosurg Psychiatry 2008; 79: 706-11.

42. Pierot L, Leclerc X, Bonafe A, Bracard S; French Matrix Registry Investigators. Endovascular treatment of intracranial aneurysms with matrix detachable coils: midterm anatomic follow-up from a prospective multicenter registry. AJNR Am J Neuroradiol 2008; 29: 57-61.

43. van Rooij WJ, de Gast AN, Sluzewski M. Results of 101 aneurysms treated with polyglycolic/polylactic acid microfilament nexus coils compared with historical controls treated with standard coils. AJNR Am J Neuroradiol 2008; 29: 991-6.

44. Standhardt H, Boecher-Schwarz H, Gruber A, Benesch T, Knosp E, Bavinzski G. Endovascular treatment of unruptured intracranial aneurysms with Guglielmi detachable coils: short- and long-term results of a single-centre series. Stroke 2008; 39: 899-904.

45. Urbach H, Dorenbeck U, von Falkenhausen M, Wilhelm K, Willinek W, Schaller C, Flacke S. Three-dimensional time-of-flight MR angiography at 3 T compared to digital subtraction angiography in the follow-up of ruptured and coiled intracranial aneurysms: a prospective study. Neuroradiology 2008; 50: 383-9.

46. Veznedaroglu E, Koebbe CJ, Siddiqui A, Rosenwasser RH. Initial experience with bioactive cerecyte detachable coils: impact on reducing recurrence rates. Neurosurgery 2008; 62: 799-805.

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3

Late reopening of

adequately coiled

intracranial aneurysms

frequency and risk factors in 400

patients with 440 aneurysms

S.P. Ferns M.E.S. Sprengers W.J.J. van Rooij W.H. van Zwam G.A.P. de Kort B.K. Velthuis J.D. Schaafsma R. van den Berg M. Sluzewski G.J.E. Rinkel C.B.L.M. Majoie

on behalf of the LOTUS study group (appendix)

3

Late reopening of

adequately coiled

intracranial aneurysms

frequency and risk factors in 400

patients with 440 aneurysms

S.P. Ferns M.E.S. Sprengers W.J.J. van Rooij W.H. van Zwam G.A.P. de Kort B.K. Velthuis J.D. Schaafsma R. van den Berg M. Sluzewski G.J.E. Rinkel C.B.L.M. Majoie

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Chapter 3 Late reopening of adequately coiled intracranial aneurysms

43

abstract

background and purpose

In aneurysms that are adequately occluded 6 months after coiling, the risk of late reopening is largely unknown. We assessed the occurrence of late aneurysm reopening and possible risk factors.

methods

From January 1995- June 2005, 1808 intracranial aneurysms were coiled in 1675 patients in 7 medical centers. At 6 months, 1066 aneurysms in 971 patients were adequately occluded. At mean 6.0 years after coiling, of the 971 patients, 400 patients with 440 aneurysms underwent 3 Tesla MRA to assess the occlusion status of the aneurysms. Proportions and corresponding 95% confidence intervals (CI) of aneurysm reopening and retreatment were calculated. Risk factors for late reopening were assessed by univariable and multivariable logistic regression analysis, including patient gender, rupture status of aneurysms, aneurysm size ≥10 mm and aneurysm location.

results

In 11 of 400 patients (2.8%, 95% CI: 1.4- 4.9%) with 440 aneurysms (2.5%, 95% CI: 1.0- 4.0%) late reopening had occurred; 3 reopened aneurysms were retreated (0.7%, 95% CI: 0.2- 1.5%). Independent predictors for late reopening were aneurysm size ≥10 mm (Odds Ratio (OR) 4.7, 95% CI: 1.3- 16.3), and location on basilar tip (OR 3.9, 95% CI: 1.1- 14.6). There were no late reopenings in 143 anterior cerebral artery aneurysms.

conclusions

In patients with aneurysms that are adequately occluded at 6 months, the yield of long-term MRA follow-up for detection of reopened aneurysms that need retreatment is very low. For these patients, extended imaging follow-up in the initial 5-10 years after coiling is generally unnecessary. Longer follow-up may be considered in potential higher-risk patients, such as patients with large or basilar tip aneurysms.

(46)

Durability of endovascular treatment for intracranial aneurysms

44

introDuction

Endovascular coiling has become an established treatment for intracranial aneurysms.1,2

A shortcoming of coiling is the possibility of aneurysm reopening over time due to coil compaction, aneurysm growth, coil migration into intraluminal thrombus or resolution of intraluminal thrombus. Reopening occurs in approximately 20% of coiled aneurysms, and about half of reopened aneurysms are retreated.3 Currently,

it is unknown for how long and how often coiled aneurysms need to be followed and whether certain subgroups carry a higher or lower risk for reopening.

Established risk factors for aneurysm reopening are large aneurysm size and low coil packing attenuation.4,5 Longer follow-up duration as a risk factor for reopening

is under debate. Some studies reported more first-time aneurysm reopenings with longer follow-up and prolonged imaging follow-up has been recommended.5,6 However,

interpretation of these studies is impeded by a wide variety in time intervals of first follow-up angiography. Reopenings that were detected on first follow up angiography some years after coiling, may have had developed much earlier. Longer follow-up duration was not associated with more aneurysm reopenings in a systematic review and in studies with fixed follow-up intervals.3,7,8

In a large multicenter patient cohort, we determined the risk of late aneurysm reopening in aneurysms with adequate occlusion at 6 months angiographic follow-up and assessed possible risk factors.

methoDs

Patients

Institutional Review Boards of the participating medical centers (St. Elisabeth Ziekenhuis Tilburg, University Medical Center Utrecht, Academic Medical Center Amsterdam, Leiden University Medical Center, VU Medical Center Amsterdam, Slotervaart Ziekenhuis Amsterdam, and Maastricht University Medical Center, all in the Netherlands) approved the study protocol. Participants provided written informed consent.

From the databases of the centers, we retrieved all patients with a ruptured or unruptured intracranial aneurysm coiled since January 1995 and had adequate aneurysm occlusion (complete occlusion or only a small neck remnant) at 6 months angiographic follow-up according to occlusion status recorded in the databases and

(47)

Chapter 3 Late reopening of adequately coiled intracranial aneurysms

45

(48)

Durability of endovascular treatment for intracranial aneurysms

46

current age between 18 and 70 years, living independently (Glasgow Outcome Scale 4 and 5)9 and no contra-indications for Magnetic Resonance Imaging at 3 Tesla (3T MR). We aimed to include 400 patients with >4.5 years of MRA follow-up in the study; the end date of the selection period was determined accordingly. We started with the patients with the longest follow-up and continued including patients until the target number of 400 was reached.

We contacted the general practitioners of all eligible patients to find out if the patient was still alive. If a patient had died, we retrieved the date and cause of death. The patients who were still alive received an invitation letter to participate in this long-term Magnetic Resonance Angiography (MRA) follow-up study with background information. Patients who did not respond to the invitation letter were contacted by phone. Participants were scanned on similar 3T MR systems in 2 of the participating centers.

mr imaging follow-up protocol

MR imaging examinations were performed on 3T systems (Intera R10; Philips Healthcare, Best, The Netherlands) by using the sensitivity encoding (SENSE) phased-array head coil (MR Imaging Devices, Gainesville, FL, USA). MR imaging protocol included axial T2-weighted fast spin echo and multiple overlapping thin slab acquisition 3D time-of-flight (MOTSA 3D-TOF) MRA sequences. Detailed descriptions of the imaging parameters have been described previously.10 Images were processed

into maximum intensity projections and volume rendered 3D images of the circle of Willis. Total MR imaging examination time was 20 minutes. This 3T MRA protocol for follow-up of coiled intracranial aneurysms has been validated in a previous study.11

mr imaging evaluation

MRI and MRA images were evaluated by 2 experienced neuroradiologists independently in 3 centers. Discrepancies were resolved in consensus. Aneurysm occlusion status was dichotomized as adequate or incomplete. In incompletely occluded aneurysms, residual aneurysm lumen was measured in 2 directions. Presence of intraluminal thrombus was assessed on axial T2-weighted images. For aneurysms that were considered incompletely occluded on follow-up MRA, images were compared to angiographic follow-up at 6 months to confirm or refute reopening, and to make a clinical advice on retreatment and extended imaging or no follow-up.

(49)

Chapter 3 Late reopening of adequately coiled intracranial aneurysms

47

statistical analysis

The first 104 included patients were described previously.10 We extended this patient

cohort to obtain more reliable data and to assess possible risk factors for late aneurysm reopening.

Proportions with 95% confidence intervals (CI) were calculated for aneurysms with reopening and for reopened aneurysms that were retreated. Patient- and aneurysm characteristics of 400 participants in this study were compared to 571 non-participants with adequate aneurysm occlusion at 6 months angiographic follow-up. Patients with aneurysm reopening were compared to patients without aneurysm reopening. The sample t-test was used for comparison of means (P≤0.05 was considered statistically significant) and odds ratios (OR) with 95% CI were calculated for binary outcome measures; patient gender, rupture status of aneurysms, aneurysm size ≥ 10 mm, posterior circulation aneurysms and basilar tip aneurysms. Subsequently, risk factors with a p-value ≤ 0.10 were included in a multivariate logistic regression model. A backward selection strategy was used and odds ratios with 95% CI were calculated.

We calculated inter-observer agreement of the dichotomized scores (adequate and incomplete occlusion) per patient in percentages.

results

baseline patient and aneurysm characteristics

Four hundred patients with 440 coiled aneurysms were included, after selecting and inviting patients treated between January 1995 and June 2005. In this time window, 1808 intracranial aneurysms in 1675 patients were treated by coiling in the 7 participating centers in the Netherlands. Of 1675 patients, 1287 with 1412 aneurysms had 6 months follow-up angiography and 1066 (75%) aneurysms in 971 patients were adequately occluded at this first angiographic follow-up. Of 971 eligible patients with 1066 aneurysms, 157 (16%) could not be traced, and 274 could not be included for a variety of reasons (Figure 1). We invited 540 patients to participate in the study to reach the target of 400 included patients, thus, 140 declined (participation grade 74%). Mean follow-up duration was 6.0 years (median 5.0, range 4.5-12.9 years).

Comparison of patient- and aneurysm characteristics of the 400 included patients (Table 1) with 571 patients that did not participate in the study resulted in a significant

(50)

Durability of endovascular treatment for intracranial aneurysms

48

MRA: Magnetic Resonance Angiography; OR: Odds Ratio; ACA: anterior cerebral artery; MCA: middle cerebral artery; ICA: internal carotid artery; - : not calculated.

* For calculation of OR for aneurysm reopening of aneurysms ≥10 mm, aneurysms <10 mm were used as reference group.

† For calculation of OR for aneurysm reopening of posterior circulation aneurysms, anterior circulation aneurysms were used as reference group. For calculation of OR for aneurysm reopening of basilar tip aneurysms, aneurysms on all other locations were used as reference group.

‡ Statistically significant

table 1. Patient- and aneurysm characteristics of all participants in long-term mra follow-up and of patients with aneurysm reopening

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