Abstract

Endovascular coil embolization is now widely used to treat cerebral aneurysms (CA) as an alternative to surgical clipping. It involves filling the aneurysmal sac with metallic coils to reduce flow, induce clotting, and promote the formation of a coil/thrombus mass which protects the aneurysm wall from hemodynamic forces and prevents rupture. However, a significant number of aneurysms are incompletely coiled leading to aneurysm regrowth and/or recanalization. Computational models of aneurysm coiling may provide important new insights into the effects of intrasaccular coil and thrombus on aneurysm wall stresses. Porcine blood and platinum coils were used to construct an in vitro coil thrombus mass (CTM) for mechanical testing. A uniaxial compression test was performed with whole blood clots and CTM, with coil packing densities (CPDs) of 10%, 20%, and 30% to obtain compressive stress/strain responses. A fourth-order polynomial mechanical response function was fit to the experimentally obtained stress/strain responses for each CPD in order to represent their mechanical properties for computational simulations. Patient-specific three-dimensional (3D) geometries of three aneurysms with simple geometry and four with complex geometry were reconstructed from digital subtraction angiography (DSA) images. The CPDs were digitally inserted in the aneurysm geometries and finite element modeling was used to determine transmural peak/mean wall stress (MWS) with and without coil packing. Reproducible stress/strain curves were obtained from compression testing of CTM and the polynomial mechanical response function was found to approximate the experimental stress/strain relationship obtained from mechanical testing to a high degree. An exponential increase in the CTM stiffness was observed with increasing CPD. Elevated wall stresses were found throughout the aneurysm dome, neck, and parent artery in simulations of the CAs with no filling. Complete, 100% filling of the aneurysms with whole blood clot and CPDs of 10%, 20%, and 30% significantly reduced MWS in simple and complex geometry aneurysms. Sequential increases in CPD resulted in significantly greater increases in MWS in simple but not complex geometry aneurysms. This study utilizes finite element analysis to demonstrate the reduction of transmural wall stress following coil embolization in patient-specific computational models of CAs. Our results provide a quantitative measure of the degree to which CPD impacts wall stress and suggest that complex aneurysmal geometries may be more resistant to coil embolization treatment. The computational modeling employed in this study serves as a first step in developing a tool to evaluate the patient-specific efficacy of coil embolization in treating CAs.

References

1.
McDougall
,
C. G.
,
Spetzler
,
R. F.
,
Zabramski
,
J. M.
,
Partovi
,
S.
,
Hills
,
N. K.
,
Nakaji
,
P.
, and
Albuquerque
,
F. C.
,
2012
, “
The Barrow Ruptured Aneurysm Trial
,”
J. Neurosurg.
,
16
(
1
), pp.
135
144
.
2.
Molyneux
,
A.
,
Kerr
,
R.
,
Stratton
,
I.
,
Sandercock
,
P.
,
Clarke
,
M.
,
Shrimpton
,
J.
, and
Holman
,
R.
,
2002
, “
International Subarachnoid Aneurysm Trial of Neurosurgical Clipping Versus Endovascular Coiling in 2143 Patients With Ruptured Intracranial Aneurysms: A Randomised Trial
,”
Lancet
,
360
(
9342
), pp.
1267
1274
.
3.
Ryttlefors
,
M.
,
Enblad
,
P.
,
Kerr
,
R. S. C.
, and
Molyneux
,
A. J.
,
2008
, “
International Subarachnoid Aneurysm Trial of Neurosurgical Clipping Versus Endovascular Coiling: Subgroup Analysis of 278 Elderly Patients
,”
Stroke
,
39
(
10
), pp.
2720
2726
.
4.
van der Schaaf
,
I.
,
Algra
,
A.
,
Wermer
,
M. J.
,
Molyneux
,
A.
,
Clarke
,
M.
,
van Gijn
,
J.
, and
Rinkel
,
G.
,
2006
, “
Endovascular Coiling Versus Neurosurgical Clipping for Patients With Aneurysmal Subarachnoid Hemorrhage
,”
Stroke
,
37
(
2
), pp.
572
573
.
5.
Molyneux
,
A. J.
,
Birks
,
J.
,
Clarke
,
A.
,
Sneade
,
M.
, and
Kerr
,
R. S. C.
,
2015
, “
The Durability of Endovascular Coiling Versus Neurosurgical Clipping of Ruptured Cerebral Aneurysms: 18 Year Follow-Up of the UK Cohort of the International Subarachnoid Aneurysm Trial (ISAT)
,”
Lancet
,
385
(
9969
), pp.
691
697
.
6.
Knap
,
D.
,
Gruszczyńska
,
K.
,
Partyka
,
R.
,
Ptak
,
D.
,
Korzekwa
,
M.
,
Zbroszczyk
,
M.
, and
Baron
,
J.
,
2013
, “
Results of Endovascular Treatment of Aneurysms Depending on Their Size, Volume and Coil Packing Density
,”
Neurol. Neurochir. Pol.
,
47
(
5
), pp.
467
475
.
7.
Berenstein
,
A.
,
Song
,
J. K.
,
Niimi
,
Y.
,
Namba
,
K.
,
Heran
,
N. S.
,
Brisman
,
J. L.
,
Nahoum
,
M. C.
,
Madrid
,
M.
,
Langer
,
D. J.
, and
Kupersmith
,
M. J.
,
2006
, “
Treatment of Cerebral Aneurysms With Hydrogel-Coated Platinum Coils (HydroCoil): Early Single-Center Experience
,”
Am. J. Neuroradiol.
,
27
(
9
), pp.
1834
1840
.https://www.ncbi.nlm.nih.gov/pubmed/17032853
8.
Raymond
,
J.
,
Guilbert
,
F.
,
Weill
,
A.
,
Georganos
,
S. A.
,
Juravsky
,
L.
,
Lambert
,
A.
,
Lamoureux
,
J.
,
Chagnon
,
M.
, and
Roy
,
D.
,
2003
, “
Long-Term Angiographic Recurrences After Selective Endovascular Treatment of Aneurysms With Detachable Coils
,”
Stroke
,
34
(
6
), pp.
1398
1403
.
9.
Johnston
,
S. C.
,
Dowd
,
C. F.
,
Higashida
,
R. T.
,
Lawton
,
M. T.
,
Duckwiler
,
G. R.
, and
Gress
,
D. R.
,
2008
, “
Predictors of Rehemorrhage After Treatment of Ruptured Intracranial Aneurysms: The Cerebral Aneurysm Rerupture After Treatment (CARAT) Study
,”
Stroke
,
39
(
1
), pp.
120
125
.
10.
Dhar
,
S.
,
Tremmel
,
M.
,
Mocco
,
J.
,
Kim
,
M.
,
Yamamoto
,
J.
,
Siddiqui
,
A. H.
,
Hopkins
,
L. N.
, and
Meng
,
H.
,
2008
, “
Morphology Parameters for Intracranial Aneurysm Rupture Risk Assessment
,”
Neurosurgery
,
63
(
2
), pp.
185
196
.
11.
Shojima
,
M.
,
Oshima
,
M.
,
Takagi
,
K.
,
Torii
,
R.
,
Hayakawa
,
M.
,
Katada
,
K.
,
Morita
,
A.
, and
Kirino
,
T.
,
2004
, “
Magnitude and Role of Wall Shear Stress on Cerebral Aneurysm: Computational Fluid Dynamic Study of 20 Middle Cerebral Artery Aneurysms
,”
Stroke
,
35
(
11
), pp.
2500
2505
.
12.
Pereira
,
V. M.
,
Brina
,
O.
,
Bijlenga
,
P.
,
Bouillot
,
P.
,
Narata
,
A. P.
,
Schaller
,
K.
,
Lovblad
,
K. O.
, and
Ouared
,
R.
,
2014
, “
Wall Shear Stress Distribution of Small Aneurysms Prone to Rupture a Case-Control Study
,”
Stroke
,
45
(
1
), pp.
261
264
.
13.
Miura
,
Y.
,
Ishida
,
F.
,
Umeda
,
Y.
,
Tanemura
,
H.
,
Suzuki
,
H.
,
Matsushima
,
S.
,
Shimosaka
,
S.
, and
Taki
,
W.
,
2013
, “
Low Wall Shear Stress Is Independently Associated With the Rupture Status of Middle Cerebral Artery Aneurysms
,”
Stroke
,
44
(
2
), pp.
519
521
.
14.
Vande Geest
,
J. P.
,
Di Martino
,
E. S.
,
Bohra
,
A.
,
Makaroun
,
M. S.
, and
Vorp
,
D. A.
,
2006
, “
A Biomechanics-Based Rupture Potential Index for Abdominal Aortic Aneurysm Risk Assessment: Demonstrative Application
,”
Ann. N. Y. Acad. Sci.
,
1085
(
1
), pp.
11
21
.
15.
Maier
,
A.
,
Gee
,
M. W.
,
Reeps
,
C.
,
Pongratz
,
J.
,
Eckstein
,
H. H.
, and
Wall
,
W. A.
,
2010
, “
A Comparison of Diameter, Wall Stress, and Rupture Potential Index for Abdominal Aortic Aneurysm Rupture Risk Prediction
,”
Ann. Biomed. Eng.
,
38
(
10
), pp.
3124
3134
.
16.
Cornejo
,
S.
,
Guzmán
,
A.
,
Valencia
,
A.
,
Rodríguez
,
J.
, and
Finol
,
E.
,
2014
, “
Flow-Induced Wall Mechanics of Patient-Specific Aneurysmal Cerebral Arteries: Nonlinear Isotropic Versus Anisotropic Wall Stress
,”
Proc. Inst. Mech. Eng. Part H
,
228
(
1
), pp.
37
48
.
17.
Lee
,
C. J.
,
Zhang
,
Y.
,
Takao
,
H.
,
Murayama
,
Y.
, and
Qian
,
Y.
,
2013
, “
A Fluid-Structure Interaction Study Using Patient-Specific Ruptured and Unruptured Aneurysm: The Effect of Aneurysm Morphology, Hypertension and Elasticity
,”
J. Biomech.
,
46
(
14
), pp.
2402
2410
.
18.
Meng
,
H.
,
Tutino
,
V. M.
,
Xiang
,
J.
, and
Siddiqui
,
A.
,
2014
, “
High WSS or Low WSS? Complex Interactions of Hemodynamics With Intracranial Aneurysm Initiation, Growth, and Rupture: Toward a Unifying Hypothesis
,”
Am. J. Neuroradiol.
,
35
(
7
), pp.
1254
1262
.
19.
Costalat
,
V.
,
Sanchez
,
M.
,
Ambard
,
D.
,
Thines
,
L.
,
Lonjon
,
N.
,
Nicoud
,
F.
,
Brunel
,
H.
,
Lejeune
,
J. P.
,
Dufour
,
H.
,
Bouillot
,
P.
,
Lhaldky
,
J. P.
,
Kouri
,
K.
,
Segnarbieux
,
F.
,
Maurage
,
C. A.
,
Lobotesis
,
K.
,
Villa-Uriol
,
M. C.
,
Zhang
,
C.
,
Frangi
,
A. F.
,
Mercier
,
G.
,
Bonafé
,
A.
,
Sarry
,
L.
, and
Jourdan
,
F.
,
2011
, “
Biomechanical Wall Properties of Human Intracranial Aneurysms Resected Following Surgical Clipping (IRRAs Project)
,”
J. Biomech.
,
44
(
15
), pp.
2685
2691
.
20.
Wang
,
H. J.
,
2002
,
Noninvasive Biomechanical Assessment of the Rupture Potential of Abdominal Aortic Aneurysms
,
University of Pittsburgh
,
Pittsburgh, PA
.
21.
Holzapfel
,
G.
,
2000
,
Nonlinear Solid Mechanics: A Continuum Approach for Engineering
,
Wiley
,
New York
.
22.
Bonet
,
J.
, and
Wood
,
R. D.
,
2008
,
Nonlinear Continuum Mechanics for Finite Element Analysis
, 2nd ed.,
Cambridge University Press
,
Cambridge, UK
.
23.
Mooney
,
M.
,
1940
, “
A Theory of Large Elastic Deformation
,”
J. Appl. Phys.
,
11
(
9
), pp.
582
592
.
24.
Rivlin
,
R. S.
, and
Saunders
,
D. W.
,
1951
, “
Large Elastic Deformations of Isotropic Materials. VII. Experiments on the Deformation of Rubber
,”
Philos. Trans. R. Soc. A
,
243
(
865
), p.
19510004
.
25.
Fung
,
Y. C.
, and
Cowin
,
S. C.
,
1994
, “
Biomechanics: Mechanical Properties of Living Tissues
,”
ASME J. Appl. Mech.
,
61
(
4
), p.
1007
.
26.
Speelman
,
L.
,
Bosboom
,
E. M. H.
,
Schurink
,
G. W. H.
,
Hellenthal
,
F. A. M. V. I.
,
Buth
,
J.
,
Breeuwer
,
M.
,
Jacobs
,
M. J.
, and
van de Vosse
,
F. N.
,
2008
, “
Patient-Specific AAA Wall Stress Analysis: 99-Percentile Versus Peak Stress
,”
Eur. J. Vasc. Endovasc. Surg.
,
36
(
6
), pp.
668
676
.
27.
Chalouhi
,
N.
,
Ali
,
M. S.
,
Jabbour
,
P. M.
,
Tjoumakaris
,
S. I.
,
Gonzalez
,
L. F.
,
Rosenwasser
,
R. H.
,
Koch
,
W. J.
, and
Dumont
,
A. S.
,
2012
, “
Biology of Intracranial Aneurysms: Role of Inflammation
,”
J. Cereb. Blood Flow Metab.
,
32
(
9
), pp.
1659
1676
.
28.
Cebral
,
J. R.
,
Mut
,
F.
,
Weir
,
J.
, and
Putman
,
C. M.
,
2011
, “
Association of Hemodynamic Characteristics and Cerebral Aneurysm Rupture
,”
Am. J. Neuroradiol.
,
32
(
2
), pp.
264
270
.
29.
Kadasi
,
L. M.
,
Dent
,
W. C.
, and
Malek
,
A. M.
,
2013
, “
Colocalization of Thin-Walled Dome Regions With Low Hemodynamic Wall Shear Stress in Unruptured Cerebral Aneurysms
,”
J. Neurosurg.
,
119
(
1
), pp.
172
179
.
30.
Kakalis
,
N. M. P.
,
Mitsos
,
A. P.
,
Byrne
,
J. V.
, and
Ventikos
,
Y.
,
2008
, “
The Haemodynamics of Endovascular Aneurysm Treatment: A Computational Modelling Approach for Estimating the Influence of Multiple Coil Deployment
,”
IEEE Trans. Med. Imaging
,
27
(
6
), pp.
814
824
.
31.
Groden
,
C.
,
Lauden
,
J.
,
Gatchell
,
S.
, and
Zeumer
,
H.
,
2001
, “
Three-Dimensional Pulsatile Flow Simulation Before and After Endovascular Coil Embolization of a Terminal Cerebral Aneurysm
,”
J. Cereb. Blood Flow Metab.
,
21
(
12
), pp.
1464
1471
.
32.
Gandhoke
,
G. S.
,
Pandya
,
Y. K.
,
Jadhav
,
A. P.
,
Jovin
,
T.
,
Friedlander
,
R. M.
,
Smith
,
K. J.
, and
Jankowitz
,
B. T.
,
2018
, “
Cost of Coils for Intracranial Aneurysms: Clinical Decision Analysis for Implementation of a Capitation Model
,”
J. Neurosurg.
,
128
, pp.
1792
1798
.
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