Abstract
Wall shear stress (WSS) is an important mediator of cardiovascular pathologies and there is a need for its reliable evaluation as a potential prognostic indicator. The purpose of this work was to develop a method that quantifies WSS from two-dimensional (2D) phase contrast magnetic resonance (PCMR) imaging derived flow waveforms, apply this method to PCMR data acquired in the abdominal aorta of healthy volunteers, and to compare PCMR-derived WSS values to values predicted from a computational fluid dynamics (CFD) simulation. The method uses PCMR-derived flow versus time waveforms constrained by the Womersley solution for pulsatile flow in a cylindrical tube. The method was evaluated for sensitivity to input parameters, intrastudy repeatability and was compared with results from a patient-specific CFD simulation. 2D-PCMR data were acquired in the aortas of healthy men (n = 12) and women (n = 15) and time-averaged WSS (TAWSS) was compared. Agreement was observed when comparing TAWSS between CFD and the PCMR flow-based method with a correlation coefficient of 0.88 (CFD: 15.0 ± 1.9 versus MRI: 13.5 ± 2.4 dyn/cm2) though comparison of WSS values between the PCMR-based method and CFD predictions indicate that the PCMR method underestimated instantaneous WSS by 3.7 ± 7.6 dyn/cm2. We found no significant difference in TAWSS magnitude between the sexes; 8.19 ± 2.25 versus 8.07 ± 1.71 dyn/cm2, p = 0.16 for men and women, respectively.
References
1.
Brooks
,
A.
,
Lelkes
,
P.
, and
Rubanyi
,
G.
, 2002
, “
Gene Expression Profiling of Human Aortic Endothelial Cells Exposed to Disturbed Flow and Steady Laminar Flow
,” Physiol. Genom.
,
9
(1
), pp. 27
–41
.10.1152/physiolgenomics.00075.20012.
Cheng
,
C.
,
Tempel
,
D.
,
Van Der Baan
,
A.
,
Krams
,
R.
,
Daemen
,
M.
,
Van Haperen
,
R.
,
Grosveld
,
F.
, and
De Crom
,
R.
, 2006
, “
Atherosclerotic Lesion Size and Vulnerability Are Determined by Patterns of Fluid Shear Stress
,” Circulation
,
113
(23
), pp. 2744
–53
.10.1161/CIRCULATIONAHA.105.5900183.
Malek
,
A.
,
Alper
,
S.
, and
Izumo
,
S.
, 1999
, “
Hemodynamic Shear Stress and Its Role in Atherosclerosis
,” JAMA
,
282
(21
), pp. 2035
–2042
.10.1001/jama.282.21.20354.
Shaaban
,
A.
, and
Duerinckx
,
A.
, 2000
, “
Wall Shear Stress and Early Atherosclerosis: A Review
,” AJR Am. J. Roentgenol.
,
174
(6
), pp. 1657
–1665
.10.2214/ajr.174.6.17416575.
Petersson
,
S.
,
Dyverfeldt
,
P.
, and
Ebbers
,
T.
, 2012
, “
Assessment of the Accuracy of MRI Wall Shear Strss Estimation Using Numerical Simulations
,” J. Magn. Reson. Imaging
,
36
(1
), pp. 128
–138
.10.1002/jmri.236106.
Chatzizisis
,
Y.
,
Jonas
,
M.
,
Edelman
,
E.
,
Feldman
,
C.
,
Stone
,
P.
, and
Coskun
,
A.
, 2007
, “
Role of Endothelial Shear Stress in the Natural History of Coronary Athersclerosis and Vascular Remodeling: Molecular Cellular and Vascular Behavior
,” J. Am. Coll. Cardiol.
,
49
(25
), p. 15
.10.1016/j.jacc.2007.02.0597.
Topper
,
J.
, and
Gimbrone
,
M.
, 1999
, “
Blood Flow and Vascular Gene Expression: Fluid Shear Stress as a Modulator of Endothelial Phenotype
,” Mol. Med. Today
, 5(1), p. 7
.10.1016/s1357-4310(98)01372-08.
Davies
,
P.
,
Krams
,
R.
, and
Spaan
,
J.
, 2005
, “
Shear Stress of the Endothelium
,” Ann. Biomed. Eng.
,
33
(12
), pp. 1714
–1718
.10.1007/s10439-005-8774-09.
Li
,
Y.
,
Chien
,
S.
, and
Haga
,
J.
, 2005
, “
Molecular Basis of the Effects of Shear Stress on Vascular Endothelial Cells
,” J. Biomech.
,
38
(10
), p. 22
.10.1016/j.jbiomech.2004.09.0310.
Pedersen
,
E.
,
Kristensen
,
I.
,
Yoganathan
,
A.
, and
Agerbaek
,
M.
, 1997
, “
Wall Shear Stress and Early Atherosclerotic Lesions in the Abdominal Aorta in Young Adults
,” Eur. J. Vasc. Surg.
,
13
(5
), p. 8
.10.1016/s1078-5884(97)80171-211.
Moore
,
J. E.
,
Glagov
,
S.
,
Zarins
,
C. K.
,
Ku
,
D. N.
, and
Xu
,
C.
, 1994
, “
Fluid Wall Shear Stress Measurements in a Model of the Human Abdominal Aorta: Oscillatory Behavior and Relationship to Atherosclerosis
,” Atheroscelerosis
,
110
(2
), pp. 225
–240
.10.1016/0021-9150(94)90207-012.
Brown
,
P.
,
Sobolev
,
B.
, and
Zelt
,
D.
, 2003
, “
The Risk of Rupture in Untreated Aneurysms: The Impact of Size, Gender, and Expansion Rate
,” J. Vasc. Surg.
,
37
(2
), pp. 280
–284
.10.1067/mva.2003.11913.
Starr
,
J.
, and
Halpern
,
V.
, 2013
, “
Abdominal Aortic Aneurysms in Women
,” J. Vasc. Surg.
,
57
(Suppl. 4), p. 3S–10S
.10.1016/j.jvs.2012.08.12514.
Harthun
,
N. L.
, 2008
, “
Current Issues in the Treatment of Women With Abdominal Aortic Aneurysm
,” Gend. Med.
,
5
(1
), pp. 36
–43
.10.1016/S1550-8579(08)80006-X15.
Grootenboer
,
N.
,
Bosch
,
J.
,
Hendriks
,
J.
, and
van Sambeek
,
M.
, 2009
, “
Epidemiology, Aetoilogy, Risk of Rupture and Treatment of Abdominal Aortic Aneurysms: Does Sex Matter?
,” Eur. J. Vasc. Endovasc. Surg.
,
38
(3
), pp. 278
–284
.10.1016/j.ejvs.2009.05.00416.
Amirbekian
,
S.
,
Long
,
R.
,
Consolini
,
M.
,
Suo
,
J.
,
Willett
,
N.
,
Fielden
,
S.
,
Giddens
,
D.
,
Taylor
,
W.
, and
Oshinski
,
J.
, 2009
, “
In Vivo Assessment of Blood Flow Patterns in Abdominal Aorta of Mice With MRI: Implications for AAA Localization
,” Am. J. Physiol. Heart Circ. Physiol.
,
297
(4
), pp. H1290–H1295.10.1152/ajpheart.00889.200817.
Taylor
,
W. R.
,
Iffrig
,
E.
,
Veneziani
,
A.
,
Oshinski
,
J. N.
, and
Smolensky
,
A.
, 2016
, “
Sex and Vascular Biomechanics: A Hypothesis for the Mechanism Underlying Differences in the Prevalence of Abdominal Aortic Aneurysms in Men and Women
,” Trans. Am. Clin. Climatol. Assoc.
,
127
, pp. 148
–161
.https://pubmed.ncbi.nlm.nih.gov/28066050/18.
Nayler
,
G.
,
Firmin
,
D. N.
, and
Longmore
,
D.
, 1986
, “
Blood Flow Imaging by Cine Magnetic Resonance
,” J. Comput. Assist. Tomogr.
,
10
(5
), pp. 715
–722
.10.1097/00004728-198609000-0000119.
Lotz
,
J.
,
Meier
,
C.
,
Leppert
,
A.
, and
Galanski
,
M.
, 2002
, “
Cardiovascular Flow Measurement With Phase-Contrast MR Imaging: Basic Facts and Implementation
,” Radiographics
,
22
(3
), pp. 651
–671
.10.1148/radiographics.22.3.g02ma1165120.
Gatehouse
,
P.
,
Keegan
,
J.
,
Crowe
,
L.
,
Masood
,
S.
,
Modiaddin
,
R.
,
Kreitner
,
K.
, and
Firmin
,
D.
, 2005
, “
Applications of Phase-Contrast Flow and Velocity Imaging in Cardiovascular MRI
,” Eur. Radiol.
,
15
(10
), pp. 20172
–22184
.10.1007/s00330-005-2829-321.
Burk
,
J.
,
Blanke
,
P.
,
Stankovic
,
Z.
,
Barker
,
A.
,
Russe
,
M.
,
Geiger
,
J.
,
Frydrychowicz
,
A.
,
Langer
,
M.
, and
Markl
,
M.
, 2012
, “
Evaluation of 3D Blood Flow Patterns and Wall Shear Stress in the Normal and Dilated Thoracic Aorta Using Flow-Sensitive 4D CMR
,” J. Cardiovasc. Magn. Reson.
,
14
(1
), p. 84
.10.1186/1532-429X-14-8422.
Pipe
,
J. G.
, 2003
, “
A Simple Measure of Flow Disorder and Wall Shear Stress in Phase Contrast MRI
,” Magn. Reson. Med.
,
49
(3
), pp. 543
–550
.10.1002/mrm.1040923.
Osinnski
,
J. N.
,
Ku
,
D. N.
,
Mukundan
,
S.
,
Loth
,
F.
, and
Pettigrew
,
R. I.
, 1995
, “
Determination of Wall Shear Stress in the Aorta With the Use of MR Phase Velocity Mapping
,” J. Magn. Reson. Imaging
,
5
(6
), pp. 640
–647
.10.1002/jmri.188005060524.
Pantos
,
I.
,
Patatoukas
,
G.
,
Efstathopoulos
,
E. P.
, and
Katritsis
,
D.
, 2007
, “
In Vivo Wall Shear Stress Measurements Using Phase-Contrast MRI
,” Expert Rev. Cardiovasc. Ther. Cardiovasc. Ther.
,
5
(5
), pp. 927
–938
.10.1586/14779072.5.5.92725.
Siegel
,
J.
, Jr.
,
Oshinski
,
J.
,
Pettigrew
,
R.
, and
Ku
,
D.
, 1996
, “
The Accuracy of Magnetic Resonance Phase Velocity Measurements in Stenotic Flow
,” J. Biomech.
,
29
(12
), pp. 1665
–1672
.10.1016/S0021-9290(96)80023-626.
Greil
,
G.
,
Geva
,
T.
,
Maier
,
S. E.
, and
Powell
,
A. J.
, 2002
, “
Effect of Acquisition Parameters on the Accuracy of Velocity Encoded Cine Magnetic Resonance Imaging Blood Flow Measurements
,” J. Magn. Reson. Imaging
,
15
(1
), pp. 47
–54
.10.1002/jmri.1002927.
Womersley
,
J. R.
, 1955
, “
Method for the Calculation of Velocity, Rate of Flow, and Viscous Drag in Arteries When the Pressure Gradient is Known
,” J. Physiol.
,
127
(3
), pp. 553
–563
.10.1113/jphysiol.1955.sp00527628.
Moore
,
J. E.
,
Maier
,
S. E.
,
Ku
,
D. N.
, and
Boesiger
,
P.
, 1994
, “
Hemodynamics in the Abdominal Aorta: A Comparison of In Vitro and In Vivo Measurements
,” J. Appl. Physiol.
,
76
(4
), pp. 1520
–1527
.10.1152/jappl.1994.76.4.152029.
Edelman
,
R.
,
Dunkle
,
E.
,
Schindler
,
N.
,
Carr
,
J.
,
Koktzoglou
,
I.
, and
Sheehan
,
J.
, 2010
, “
Quiescent-Interval Single-Shot Unenhanced Magnetic Resonance Angiography of Peripheral Vascular Disease: Technical Considerations and Clinical Feasibility
,” Magn. Reson. Imaging
,
63
(4
), pp. 951
–958
.10.1002/mrm.2228730.
Bidhult
,
S.
,
Carlsson
,
M.
,
Steding-Ehrenborg
,
K.
,
Arheden
,
H.
, and
Heiberg
,
E.
, 2014
, “
A New Method for Vessel Segmentation Based on a Priori Input From Medical Expertise in Cine Phase-Contrast Magnetic Resonance Imaging
,” J. Cardiovasc. Magn. Reson
., 16, p. 355
.10.1186/1532-429X-16-S1-P35531.
He
,
X.
,
Ku
,
D.
, and
Moore
,
J.
, 1993
, “
Simple Calculation of the Velocity Profiles for Pulsatile Flow in a Blood Vessel Using Mathematica
,” Ann. Biomed. Eng.
,
21
(1
), pp. 45
–49
.10.1007/BF0236816332.
Timmins
,
L.
,
Molony
,
D.
,
Eshtehardi
,
P.
,
McDaniel
,
M.
,
Oshinski
,
J.
,
Samady
,
H.
, and
Giddens
,
D.
, 2015
, “
Focal Association Between Wall Shear Stress and Clinical Coronary Artery Disease Progression
,” Ann. Biomed. Eng.
,
43
(1
), pp. 94
–106
.10.1007/s10439-014-1155-933.
McBridge
,
G.
, 2005
, A Proposal for Strength-of-Agreement Criteria for Lin's Concordance Correlation Coefficient
,
NIWA
, Hamilton, New Zealand.34.
Gao
,
X.
,
Starmer
,
J.
, and
Martin
,
E. R.
, 2008
, “
A Multiple Testing Correction Method for Genetic Association Studies Using Correlated Single Nucleotide Polymorphisms
,” Genet. Epidemiol.
,
32
(4
), pp. 361
–369
.10.1002/gepi.2031035.
Oyre
,
S.
,
Ringgaard
,
S.
,
Kozerke
,
S.
,
Paaske
,
W. P.
,
Scheidegger
,
M. B.
,
Boesiger
,
P.
, and
Pedersen
,
E. M.
, 1998
, “
Quantitation of Circumferential Subpixel Vessel Wall Position and Wall Shear Stress by Multiple Sectored Three-Dimensional Paraboloid Modeling of Velocity Encoded Cine MR
,” Magn. Reson. Med.
,
40
(5
), pp. 645
–655
.10.1002/mrm.191040050236.
Perinajová
,
R.
,
Juffermans
,
J.
,
Westenberg
,
J.
,
van der Palen
,
R.
,
van den Boogaard
,
P.
,
Lamb
,
H.
, and
Kenjereš
,
S.
, 2021
, “
Geometrically Induced Wall Shear Stress Variability in CFD-MRI Coupled Simulations of Blood Flow in the Thoracic Aortas
,” Comput. Biol. Med.
,
133
, p. 104385
.10.1016/j.compbiomed.2021.10438537.
Ku
,
D.
,
Giddens
,
D.
,
Zarins
,
C.
, and
Glagov
,
S.
, 1985
, “
Pulsatile Flow and Atherosclerosis in the Human Carotid Bifurcation. Positive Correlation Between Plaque Location and Low Oscillating Shear Stress
,” Aeteriosclerosis
,
5
(3
), pp. 293
–302
.10.1161/01.ATV.5.3.29338.
Nguyen
,
N.
, and
Haque
,
A.
, 1990
, “
Effect of Hemodynamics Factors on Atherosclerosis in the Abdominal Aorta
,” Atheroscelerosis
,
84
(1
), pp. 33
–39
.10.1016/0021-9150(90)90005-439.
Pedersen
,
E. M.
,
Oyre
,
S.
,
Agerbæk
,
M.
,
Kristensen
,
I. B.
,
Ringgaard
,
S.
,
Boesiger
,
P.
, and
Paaske
,
W. P.
, 1999
, “
Distribution of Early Atherosclerotic Lesions in the Human Abdominal Aorta Correlates With Wall Shear Stresses Measured In Vivo
,” Eur. J. Vasc. Surg.
,
18
(4
), pp. 328
–333
.10.1053/ejvs.1999.091340.
Cecchi
,
E.
,
Valente
,
S.
,
Lazzeri
,
C.
,
Gensini
,
G.
,
Abbate
,
R.
,
Mannini
,
L.
, and
Giglioli
,
C.
, 2011
, “
Role of Hemodynamic Shear Stress in Cardiovascular Disease
,” Atherosclerosis
,
214
(2
), pp. 249
–256
.10.1016/j.atherosclerosis.2010.09.00841.
Peiffer
,
V.
,
Sherwin
,
S.
, and
Weinberg
,
P.
, 2013
, “
Does Low and Oscillatory Wall Shear Stress Correlate Spatially With Early Atherosclerosis? A Systematic Review
,” Cardiovasc. Res.
,
99
(2
), pp. 242
–250
.10.1093/cvr/cvt04442.
Morris
,
P. D.
,
Narracott
,
A.
,
von Tengg-Kobligk
,
H.
,
Silva Soto
,
D. A.
,
Hsiao
,
S.
,
Lungu
,
A.
,
Evans
,
P.
,
Bressloff
,
N. W.
,
Lawford
,
P. V.
,
Hose
,
D. R.
, and
Gunn
,
J. P.
, 2016
, “
Computational Fluid Dynamics Modelling in Cardiovascular Medicine
,” Heart
,
102
(1
), pp. 18
–28
.10.1136/heartjnl-2015-30804443.
S
,
J.
,
J
,
O.
, and
DP
,
G.
, 2003
, “
Effects of Wall Motion and Compliance on Flow Patterns in the Ascending Aorta
,” ASME J. Biomech. Eng.
,
125
(3
), pp. 347
–354
.10.1115/1.157433244.
Cibis
,
M.
,
Potters
,
W.
,
Gijsen
,
F.
,
Marquering
,
H.
,
van Ooij
,
P.
,
VanBavel
,
E.
,
Wentzel
,
J.
, and
Nederveen
,
A.
, 2016
, “
The Effect of Spatial and Temporal Resolution of Cine Phase Contrast MRI on Wall Shear Stress and Oscillatory Shear Index Assessment
,” PLoS One
,
11
(9
), p. e0163316
.10.1371/journal.pone.016331645.
Cibis
,
M.
,
Potters
,
W.
,
Selwaness
,
M.
,
Gijsen
,
F.
,
Franco
,
O.
,
Lorza
,
A.
,
Bruijne
,
M.
,
Hofman
,
A.
,
Lugt
,
A.
,
Nederveen
,
A.
, and
Wentzel
,
J.
, 2016
, “
Relation Between Wall Shear Stress and Carotid Artery Wall Thickening MRI Versus CFD
,” J. Biomech.
,
49
(5
), pp. 735
–741
.10.1016/j.jbiomech.2016.02.00446.
Corso
,
P.
,
Walheim
,
J.
,
Dillinger
,
H.
,
Giannakopoulos
,
G.
,
Gülan
,
U.
,
Frouzakis
,
C.
,
Kozerke
,
S.
, and
Holzner
,
M.
, 2021
, “
Toward an Accurate Estimation of Wall Shear Stress From 4D Flow Magnetic Resonance Downstream of a Severe Stenosis
,” Magn. Reson. Med.
,
86
(3
), pp. 1531
–1543
.10.1002/mrm.2879547.
Gharahi
,
H.
,
Zambrano
,
B.
,
Zhu
,
D.
,
DeMarco
,
J.
, and
Baek
,
S.
, 2016
, “
Computational Fluid Dynamic Simulation of Human Carotid Artery Bifurcation Based on Anatomy and Volumetric Blood Flow Rate Measured With Magnetic Resonance Imaging
,” Int. J. Adv. Eng. Sci. Appl. Math.
,
8
(1
), pp. 46
–60
.10.1007/s12572-016-0161-648.
Szajer
,
J.
, and
Ho-Shon
,
K.
, 2018
, “
A Comparison of 4D Flow MRI-Derived Wall Shear Stress With Computational Fluid Dynamics Methods for Intracranial Aneurysms and Carotid Bifurcations—A Review
,” Magn. Reson. Imaging
,
48
, pp. 62
–69
.10.1016/j.mri.2017.12.00549.
Köhler
,
U.
,
Marshall
,
I.
,
Robertson
,
M.
,
Long
,
Q.
,
Xu
,
X.
, and
Hoskins
,
P.
, 2001
, “
MRI Measurement of Wall Shear Stress Vectors in Bifurcation Models and Comparison With CFD Predictions
,” J. Magn. Reson. Imaging
,
14
(5
), pp. 563
–573
.10.1002/jmri.122050.
Wanhainen
,
A.
,
Mani
,
K.
, and
Svensjo
,
S.
, 2008
, “
Screening for AAA – Areas Where Information is Still Inadequate
,” Scand. J. Surg.
,
97
(2
), pp. 131
–135
.10.1177/14574969080970021151.
Lo
,
R.
,
Bensley
,
R.
,
Hamdan
,
A.
,
Wyers
,
M.
,
Adams
,
J.
, and
Schermerhorn
,
M.
, 2013
, “
Gender Differences in Abdominal Aortic Aneurysm Presentation, Repair, and Mortality in the Vascular Study Group of New England
,” J. Vasc. Surg.
,
57
(5
), pp. 1261
–1268.e5
.10.1016/j.jvs.2012.11.03952.
Norman
,
P.
, and
Powell
,
J.
, 2007
, “
Abdominal Aortic Aneurysm: The Prognosis in Women is Worse Than in Men
,” Circulation
,
115
(22
), pp. 2865
–2869
.10.1161/CIRCULATIONAHA.106.67185953.
Larsson
,
E.
,
Labruto
,
F.
,
Gasser
,
T. C.
,
Swedenborg
,
J.
, and
Hultgren
,
R.
, 2011
, “
Analysis of Aortic Wall Stress and Rupture Risk in Patients With Abdominal Aortic Aneurysm With a Gender Perspective
,” J. Vasc. Surg.
,
54
(2
), pp. 295
–299
.10.1016/j.jvs.2010.12.05354.
Iffrig
,
E.
,
Wilson
,
J. S.
,
Zhong
,
X.
, and
Oshinski
,
J. N.
, 2019
, “
Demonstration of Circumferential Heterogeneity in Displacement and Strain in the Abdominal Aortic Wall by Spiral Cine DENSE MRI
,” J. Magn. Reson. Imaging
,
49
(3
), pp. 731
–743
.10.1002/jmri.2630455.
Motomiya
,
M.
, and
Karino
,
T.
, 1984
, “
Flow Patterns in the Human Carotid Artery Bifurcation
,” Stroke
,
15
(1
), pp. 50
–56
.10.1161/01.STR.15.1.5056.
Dua
,
M.
, and
Dalman
,
R.
, 2010
, “
Hemodynamic Influences on Abdominal Aortic Aneurysm Disease: Application to Aneurysm Pathophysiology
,” Vascul. Pharmacol.
,
53
(1–2
), pp. 11
–21
.10.1016/j.vph.2010.03.00457.
Vignon-Clementel
,
I. E.
,
Alberto Figueroa
,
C.
,
Jansen
,
K. E.
, and
Taylor
,
C. A.
, 2006
, “
Outflow Boundary Conditions for Three-Dimensional Finite Element Modeling of Blood Flow and Pressure in Arteries
,” Comput. Methods Appl. Mech. Eng.
,
195
(29–32
), pp. 3776
–3796
.10.1016/j.cma.2005.04.014Copyright © 2022 by ASME
You do not currently have access to this content.
