Abstract

Despite the important advancements in the stent technology for the treatment of diseased coronary arteries, major complications still affect the postoperative long-term outcome. The stent-induced flow disturbances, and especially the altered wall shear stress (WSS) profile at the strut level, play an important role in the pathophysiological mechanisms leading to stent thrombosis (ST) and in-stent restenosis (ISR). In this context, the analysis of the WSS topological skeleton is gaining more and more interest by extending the current understanding of the association between local hemodynamics and vascular diseases. This study aims to analyze the impact that a deployed coronary stent has on the WSS topological skeleton. Computational fluid dynamics (CFD) simulations were performed in three stented human coronary artery geometries reconstructed from clinical images. The selected cases presented stents with different designs (i.e., two contemporary drug-eluting stents and one bioresorbable scaffold) and included regions with stent malapposition or overlapping. A recently proposed Eulerian-based approach was applied to analyze the WSS topological skeleton features. The results highlighted that the presence of single or multiple stents within a coronary artery markedly impacts the WSS topological skeleton. In particular, repetitive patterns of WSS divergence were observed at the luminal surface, highlighting a WSS contraction action exerted proximal to the stent struts and a WSS expansion action distal to the stent struts. This WSS action pattern was independent from the stent design. In conclusion, these findings could contribute to a deeper understanding of the hemodynamics-driven processes underlying ST and ISR.

References

1.
Otake
,
H.
,
2021
, “
Stent Edge Restenosis—An Inevitable Drawback of Stenting?
,”
Circ. J.: Off. J. Jpn. Circ. Soc.
,
85
(
11
), pp.
1969
1971
.10.1253/circj.CJ-21-0581
2.
Tomberli
,
B.
,
Mattesini
,
A.
,
Baldereschi
,
G. I.
, and
Di Mario
,
C.
,
2018
, “
A Brief History of Coronary Artery Stents
,”
Rev. Esp. Cardiol. (Engl. Ed.)
,
71
(
5
), pp.
312
319
.10.1016/j.recesp.2017.11.016
3.
Stefanini
,
G.
,
Byrne
,
R.
,
Windecker
,
S.
, and
Kastrati
,
A.
,
2017
, “
State of the Art: Coronary Artery Stents - Past, Present and Future
,”
EuroIntervention
,
13
(
6
), pp.
706
716
.10.4244/EIJ-D-17-00557
4.
Reejhsinghani
,
R.
, and
Lotfi
,
A. S.
,
2015
, “
Prevention of Stent Thrombosis: Challenges and Solutions
,”
Vasc. Health Risk Manag.
,
11
, pp.
93
106
.10.2147/VHRM.S43357
5.
Byrne
,
R. A.
,
Joner
,
M.
, and
Kastrati
,
A.
,
2015
, “
Stent Thrombosis and Restenosis: What Have We Learned and Where Are We Going? The Andreas Grüntzig Lecture ESC 2014
,”
Eur. Heart J.
,
36
(
47
), pp.
3320
3331
.10.1093/eurheartj/ehv511
6.
Shlofmitz
,
E.
,
Iantorno
,
M.
, and
Waksman
,
R.
,
2019
, “
Restenosis of Drug-Eluting Stents: A New Classification System Based on Disease Mechanism to Guide Treatment and State-of-the-Art Review
,”
Circ.: Cardiovasc. Interventions
,
12
(
8
), p.
e007023
.10.1161/CIRCINTERVENTIONS.118.007023
7.
Koskinas
,
K. C.
,
Chatzizisis
,
Y. S.
,
Antoniadis
,
A. P.
, and
Giannoglou
,
G. D.
,
2012
, “
Role of Endothelial Shear Stress in Stent Restenosis and Thrombosis: Pathophysiologic Mechanisms and Implications for Clinical Translation
,”
J. Am. Coll. Cardiol.
,
59
(
15
), pp.
1337
1349
.10.1016/j.jacc.2011.10.903
8.
Ng
,
J.
,
Bourantas
,
C. V.
,
Torii
,
R.
,
Ang
,
H. Y.
,
Tenekecioglu
,
E.
,
Serruys
,
P. W.
, and
Foin
,
N.
,
2017
, “
Local Hemodynamic Forces After Stenting: Implications on Restenosis and Thrombosis
,”
Arterioscler., Thromb., Vasc. Biol.
,
37
(
12
), pp.
2231
2242
.10.1161/ATVBAHA.117.309728
9.
Kolandaivelu
,
K.
,
Swaminathan
,
R.
,
Gibson
,
W. J.
,
Kolachalama
,
V. B.
,
Nguyen-Ehrenreich
,
K. L.
,
Giddings
,
V. L.
,
Coleman
,
L.
,
Wong
,
G. K.
, and
Edelman
,
E. R.
,
2011
, “
Stent Thrombogenicity Early in High-Risk Interventional Settings Is Driven by Stent Design and Deployment and Protected by Polymer-Drug Coatings
,”
Circulation
,
123
(
13
), pp.
1400
1409
.10.1161/CIRCULATIONAHA.110.003210
10.
Nguyen
,
D. T.
,
Smith
,
A. F.
, and
Jiménez
,
J. M.
,
2021
, “
Stent Strut Streamlining and Thickness Reduction Promote Endothelialization
,”
J. R. Soc. Interface
,
18
(
181
), p.
20210023
.10.1098/rsif.2021.0023
11.
Mazzi
,
V.
,
Morbiducci
,
U.
,
Calò
,
K.
,
De Nisco
,
G.
,
Lodi Rizzini
,
M.
,
Torta
,
E.
,
Caridi
,
G. C. A.
,
Chiastra
,
C.
, and
Gallo
,
D.
,
2021
, “
Wall Shear Stress Topological Skeleton Analysis in Cardiovascular Flows: Methods and Applications
,”
Mathematics
,
9
(
7
), p.
720
.10.3390/math9070720
12.
Mazzi
,
V.
,
Gallo
,
D.
,
Calò
,
K.
,
Najafi
,
M.
,
Khan
,
M. O.
,
De Nisco
,
G.
,
Steinman
,
D. A.
, and
Morbiducci
,
U.
,
2019
, “
A Eulerian Method to Analyze Wall Shear Stress Fixed Points and Manifolds in Cardiovascular Flows
,”
Biomech. Model. Mechanobiol.
,
9
(
5
), pp.
1403
1423
.10.1007/s10237-019-01278-3
13.
Arzani
,
A.
, and
Shadden
,
S. C.
,
2018
, “
Wall Shear Stress Fixed Points in Cardiovascular Fluid Mechanics
,”
J. Biomech.
,
73
, pp.
145
152
.10.1016/j.jbiomech.2018.03.034
14.
Arzani
,
A.
,
Gambaruto
,
A. M.
,
Chen
,
G.
, and
Shadden
,
S. C.
,
2016
, “
Lagrangian Wall Shear Stress Structures and Near-Wall Transport in High-Schmidt-Number Aneurysmal Flows
,”
J. Fluid Mech.
,
790
, pp.
158
172
.10.1017/jfm.2016.6
15.
Mazzi
,
V.
,
De Nisco
,
G.
,
Hoogendoorn
,
A.
,
Calò
,
K.
,
Chiastra
,
C.
,
Gallo
,
D.
,
Steinman
,
D. A.
,
Wentzel
,
J. J.
, and
Morbiducci
,
U.
,
2021
, “
Early Atherosclerotic Changes in Coronary Arteries Are Associated With Endothelium Shear Stress Contraction/Expansion Variability
,”
Ann. Biomed. Eng.
,
49
(
9
), pp.
2606
2621
.10.1007/s10439-021-02829-5
16.
Morbiducci
,
U.
,
Mazzi
,
V.
,
Domanin
,
M.
,
De Nisco
,
G.
,
Vergara
,
C.
,
Steinman
,
D. A.
, and
Gallo
,
D.
,
2020
, “
Wall Shear Stress Topological Skeleton Independently Predicts Long-Term Restenosis After Carotid Bifurcation Endarterectomy
,”
Ann. Biomed. Eng.
,
48
(
12
), pp.
2936
2949
.10.1007/s10439-020-02607-9
17.
De Nisco
,
G.
,
Tasso
,
P.
,
Calò
,
K.
,
Mazzi
,
V.
,
Gallo
,
D.
,
Condemi
,
F.
,
Farzaneh
,
S.
,
Avril
,
S.
, and
Morbiducci
,
U.
,
2020
, “
Deciphering Ascending Thoracic Aortic Aneurysm Hemodynamics in Relation to Biomechanical Properties
,”
Med. Eng. Phys.
,
82
, pp.
119
129
.10.1016/j.medengphy.2020.07.003
18.
Candreva
,
A.
,
Pagnoni
,
M.
,
Rizzini
,
M. L.
,
Mizukami
,
T.
,
Gallinoro
,
E.
,
Mazzi
,
V.
,
Gallo
,
D.
,
2021
, “
Risk of Myocardial Infarction Based on Endothelial Shear Stress Analysis Using Coronary Angiography
,”
Atherosclerosis
, 342, pp. 28–35.10.1016/j.atherosclerosis.2021.11.010
19.
Chiastra
,
C.
,
Morlacchi
,
S.
,
Gallo
,
D.
,
Morbiducci
,
U.
,
Cárdenes
,
R.
,
Larrabide
,
I.
, and
Migliavacca
,
F.
,
2013
, “
Computational Fluid Dynamic Simulations of Image-Based Stented Coronary Bifurcation Models
,”
J. R. Soc. Interface
,
10
(
84
), p.
20130193
.10.1098/rsif.2013.0193
20.
Morlacchi
,
S.
,
Colleoni
,
S. G.
,
Cárdenes
,
R.
,
Chiastra
,
C.
,
Diez
,
J. L.
,
Larrabide
,
I.
, and
Migliavacca
,
F.
,
2013
, “
Patient-Specific Simulations of Stenting Procedures in Coronary Bifurcations: Two Clinical Cases
,”
Med. Eng. Phys.
,
35
(
9
), pp.
1272
1281
.10.1016/j.medengphy.2013.01.007
21.
Cerrato
,
E.
,
Barbero
,
U.
,
Gil Romero
,
J. A.
,
Quadri
,
G.
,
Mejia-Renteria
,
H.
,
Tomassini
,
F.
,
Ferrari
,
F.
,
Varbella
,
F.
,
Gonzalo
,
N.
, and
Escaned
,
J.
,
2019
, “
MagmarisTM Resorbable Magnesium Scaffold: State-of-Art Review
,”
Future Cardiol.
,
15
(
4
), pp.
267
279
.10.2217/fca-2018-0081
22.
Chiastra
,
C.
,
Montin
,
E.
,
Bologna
,
M.
,
Migliori
,
S.
,
Aurigemma
,
C.
,
Burzotta
,
F.
,
Celi
,
S.
,
Dubini
,
G.
,
Migliavacca
,
F.
, and
Mainardi
,
L.
,
2017
, “
Reconstruction of Stented Coronary Arteries From Optical Coherence Tomography Images: Feasibility, Validation, and Repeatability of a Segmentation Method
,”
PLoS One
,
12
(
6
), p.
e0177495
.10.1371/journal.pone.0177495
23.
Migliori
,
S.
,
Chiastra
,
C.
,
Bologna
,
M.
,
Montin
,
E.
,
Dubini
,
G.
,
Aurigemma
,
C.
,
Fedele
,
R.
,
Burzotta
,
F.
,
Mainardi
,
L.
, and
Migliavacca
,
F.
,
2017
, “
A Framework for Computational Fluid Dynamic Analyses of Patient-Specific Stented Coronary Arteries From Optical Coherence Tomography Images
,”
Med. Eng. Phys.
,
47
, pp.
105
116
.10.1016/j.medengphy.2017.06.027
24.
Chiastra
,
C.
,
Migliori
,
S.
,
Burzotta
,
F.
,
Dubini
,
G.
, and
Migliavacca
,
F.
,
2018
, “
Patient-Specific Modeling of Stented Coronary Arteries Reconstructed From Optical Coherence Tomography: Towards a Widespread Clinical Use of Fluid Dynamics Analyses
,”
J. Cardiovasc. Transl. Res.
,
11
(
2
), pp.
156
172
.10.1007/s12265-017-9777-6
25.
Davies
,
J. E.
,
Whinnett
,
Z. I.
,
Francis
,
D. P.
,
Manisty
,
C. H.
,
Aguado-Sierra
,
J.
,
Willson
,
K.
,
Foale
,
R. A.
,
2006
, “
Evidence of a Dominant Backward-Propagating ‘Suction’ Wave Responsible for Diastolic Coronary Filling in Humans, Attenuated in Left Ventricular Hypertrophy
,”
Circulation
,
113
(
14
), pp.
1768
1778
.10.1161/CIRCULATIONAHA.105.603050
26.
Lodi Rizzini
,
M.
,
Gallo
,
D.
,
De Nisco
,
G.
,
D'Ascenzo
,
F.
,
Chiastra
,
C.
,
Bocchino
,
P. P.
,
Piroli
,
F.
,
De Ferrari
,
G. M.
, and
Morbiducci
,
U.
,
2020
, “
Does the Inflow Velocity Profile Influence Physiologically Relevant Flow Patterns in Computational Hemodynamic Models of Left Anterior Descending Coronary Artery?
,”
Med. Eng. Phys.
,
82
, pp.
58
69
.10.1016/j.medengphy.2020.07.001
27.
van der Giessen
,
A. G.
,
Groen
,
H. C.
,
Doriot
,
P.-A.
,
de Feyter
,
P. J.
,
van der Steen
,
A. F. W.
,
van de Vosse
,
F. N.
,
Wentzel
,
J. J.
, and
Gijsen
,
F. J. H.
,
2011
, “
The Influence of Boundary Conditions on Wall Shear Stress Distribution in Patients Specific Coronary Trees
,”
J. Biomech.
,
44
(
6
), pp.
1089
1095
.10.1016/j.jbiomech.2011.01.036
28.
Garth
,
C.
,
Tricoche
,
X.
, and
Scheuermann
,
G.
,
2004
, “
Tracking of Vector Field Singularities in Unstructured 3D Time-Dependent Datasets
,”
IEEE Visualization 2004
, Austin, TX, Oct. 10–15, pp.
329
336
.10.1109/VISUAL.2004.107
29.
Gambaruto
,
A. M.
, and
João
,
A. J.
,
2012
, “
Computers & Fluids Flow Structures in Cerebral Aneurysms
,”
Comput. Fluids
,
65
, pp.
56
65
.10.1016/j.compfluid.2012.02.020
30.
Cornelissen
,
A.
, and
Vogt
,
F. J.
,
2019
, “
The Effects of Stenting on Coronary Endothelium From a Molecular Biological View: Time for Improvement?
,”
J. Cell. Mol. Med.
,
23
(
1
), pp.
39
46
.10.1111/jcmm.13936
31.
Asahara
,
T.
,
Masuda
,
H.
,
Takahashi
,
T.
,
Kalka
,
C.
,
Pastore
,
C.
,
Silver
,
M.
,
Kearne
,
M.
,
Magner
,
M.
, and
Isner
,
J. M.
,
1999
, “
Bone Marrow Origin of Endothelial Progenitor Cells Responsible for Postnatal Vasculogenesis in Physiological and Pathological Neovascularization
,”
Circ. Res.
,
85
(
3
), pp.
221
228
.10.1161/01.RES.85.3.221
32.
Lindner
,
V.
,
Majack
,
R. A.
, and
Reidy
,
M. A.
,
1990
, “
Basic Fibroblast Growth Factor Stimulates Endothelial Regrowth and Proliferation in Denuded Arteries
,”
J. Clin. Invest.
,
85
(
6
), pp.
2004
2008
.10.1172/JCI114665
33.
Van der Heiden
,
K.
,
Gijsen
,
F. J. H.
,
Narracott
,
A.
,
Hsiao
,
S.
,
Halliday
,
I.
,
Gunn
,
J.
,
Wentzel
,
J. J.
, and
Evans
,
P. C.
,
2013
, “
The Effects of Stenting on Shear Stress: Relevance to Endothelial Injury and Repair
,”
Cardiovasc. Res.
,
99
(
2
), pp.
269
275
.10.1093/cvr/cvt090
34.
Chiu
,
J.-J.
, and
Chien
,
S.
,
2011
, “
Effects of Disturbed Flow on Vascular Endothelium: Pathophysiological Basis and Clinical Perspectives
,”
Physiol. Rev.
,
91
(
1
), pp.
327
387
.10.1152/physrev.00047.2009
35.
Munk
,
P. S.
,
Butt
,
N.
, and
Larsen
,
A. I.
,
2011
, “
Endothelial Dysfunction Predicts Clinical Restenosis After Percutaneous Coronary Intervention
,”
Scand. Cardiovasc. J.
,
45
(
3
), pp.
139
145
.10.3109/14017431.2011.564646
36.
Beier
,
S.
,
Ormiston
,
J.
,
Webster
,
M.
,
Cater
,
J.
,
Norris
,
S.
,
Medrano-Gracia
,
P.
,
Young
,
A.
, and
Cowan
,
B.
,
2016
, “
Hemodynamics in Idealized Stented Coronary Arteries: Important Stent Design Considerations
,”
Ann. Biomed. Eng.
,
44
(
2
), pp.
315
329
.10.1007/s10439-015-1387-3
37.
Hsiao
,
S. T.
,
Spencer
,
T.
,
Boldock
,
L.
,
Prosseda
,
S. D.
,
Xanthis
,
I.
,
Tovar-Lopez
,
F. J.
,
Van Beusekom
,
H. M. M.
,
2016
, “
Endothelial Repair in Stented Arteries Is Accelerated by Inhibition of Rho-Associated Protein Kinase
,”
Cardiovasc. Res.
,
112
(
3
), pp.
689
701
.10.1093/cvr/cvw210
38.
Lagache
,
M.
,
Coppel
,
R.
,
Finet
,
G.
,
Derimay
,
F.
,
Pettigrew
,
R. I.
,
Ohayon
,
J.
, and
Malvè
,
M.
,
2021
, “
Impact of Malapposed and Overlapping Stents on Hemodynamics: A 2D Parametric Computational Fluid Dynamics Study
,”
Mathematics
,
9
(
8
), p.
795
.10.3390/math9080795
39.
Jiménez
,
J. M.
, and
Davies
,
P. F.
,
2009
, “
Hemodynamically Driven Stent Strut Design
,”
Ann. Biomed. Eng.
,
37
(
8
), pp.
1483
1494
.10.1007/s10439-009-9719-9
40.
Tarrahi
,
I.
,
Colombo
,
M.
,
Hartman
,
E.
,
Forero
,
M. T.
,
Torii
,
R.
,
Chiastra
,
C.
,
Daemen
,
J.
, and
Gijsen
,
F.
,
2020
, “
Impact of Bioresorbable Scaffold Design Characteristics on Local Haemodynamic Forces: An Ex Vivo Assessment With Computational Fluid Dynamics Simulations
,”
EuroIntervention
,
16
(
11
), pp.
E930
E937
.10.4244/EIJ-D-19-00657
41.
Chiastra
,
C.
,
Migliavacca
,
F.
,
Martinez
,
M. A.
, and
Malve
,
M.
,
2014
, “
On the Necessity of Modelling Fluid-Structure Interaction for Stented Coronary Arteries
,”
J. Mech. Behav. Biomed. Mater.
,
34
, pp.
217
230
.10.1016/j.jmbbm.2014.02.009
42.
Zeng
,
D.
,
Ding
,
Z.
,
Friedman
,
M. H.
, and
Ethier
,
C. R.
,
2003
, “
Effects of Cardiac Motion on Right Coronary Artery Hemodynamics
,”
Ann. Biomed. Eng.
,
31
(
4
), pp.
420
429
.10.1114/1.1560631
You do not currently have access to this content.