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Journal of Biomechanics
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art ic l e i nf o
a b s t r a c t
Article history:
Accepted 27 April 2015
We present a computational method for calculating the distribution of wall shear stress (WSS) in the
aorta based on a velocity eld obtained from two-dimensional (2D) phase-contrast magnetic resonance
imaging (PC-MRI) data and a nite-element method. The WSS vector was obtained from a global leastsquares stress-projection method. The method was benchmarked against the Womersley model, and the
robustness was assessed by changing resolution, noise, and positioning of the vessel wall. To showcase
the applicability of the method, we report the axial, circumferential and magnitude of the WSS using invivo data from ve volunteers. Our results showed that WSS values obtained with our method were in
good agreement with those obtained from the Womersley model. The results for the WSS contour means
showed a systematic but decreasing bias when the pixel size was reduced. The proposed method proved
to be robust to changes in noise level, and an incorrect position of the vessel wall showed large errors
when the pixel size was decreased. In volunteers, the results obtained were in good agreement with
those found in the literature. In summary, we have proposed a novel image-based computational method
for the estimation of WSS on vessel sections with arbitrary cross-section geometry that is robust in the
presence of noise and boundary misplacements.
& 2015 Elsevier Ltd. All rights reserved.
Keywords:
2D CINE PC-MRI
Wall shear stress
Finite elements
Fluid mechanics
Flow quantication
1. Introduction
Two-dimensional cine phase-contrast magnetic resonance imaging (2D CINE PC-MRI) and three-dimensional (3D) CINE PC-MRI
have been used non-invasively to obtain qualitative and quantitative
information on the cardiovascular system. Several numerical procedures have recently been proposed to evaluate ow patterns,
determine the wall shear stress (WSS) distribution, and calculate
pressure difference maps (Oshinski et al., 1995; Tyszka et al., 2000;
Ebbers et al., 2001; Barker et al., 2010; Bock et al., 2010, 2011). These
methods have shown the potential of 2D and 3D CINE PC-MRI for
assessing different cardiovascular diseases (Wigstrm et al., 1999;
n
Correspondence to: Radiology Department, School of Medicine and Biomedical
Imaging Center. Ponticia Universidad Catlica de Chile. Marcoleta 367, Santiago,
Chile. Tel.: 56 2 23548272; fax: 56 2 23548468.
E-mail address: suribe@med.puc.cl (S. Uribe).
http://dx.doi.org/10.1016/j.jbiomech.2015.04.038
0021-9290/& 2015 Elsevier Ltd. All rights reserved.
1818
2. Theory
2.1. Computation of the wall shear stress using a nite-element
method
The shear stress vector and magnitude at the vessel wall were
computed using the procedure described in the electronic supplementary material (see Appendix: nite element formulation),
which we briey summarize next. The velocity eld was obtained
at a discrete set of pixels using 2D CINE PC-MRI. Using linear triangular nite-element interpolations, the velocity-component
eld uiFEM (x,t ) is continuously described by the expression:
uiFEM (x, t ) =
N A (x ) viA (t ),
(1)
S (x, t ) =
N A (x ) A (t ),
(2)
where A is the nodal smoothed value of the stress components obtained from a global least-squares minimization of the
stress L2 error. Once all the shear-component elds are obtained,
the shear stress tensor at any point in the domain of interest, and
particularly at the domain boundaries (i.e. vessel wall), can be
estimated using Eq. (2). Let n be the inward unit vector normal to
the vessel wall at a particular point of interest. Then, the WSS
vector corresponding to the shear stress tensor takes the form:
(3)
t = n .
For the purpose of this work, we consider the axial, circumferential and magnitude of the WSS vector projected over the
t proy = n
t
n .
(4)
vel (x , y , t ) =
) ,
J0 r (x , y ) i 3/2
A0
1
v
R 2 r (x , y )2 + Re PGm (t )
1
3/2
4
i
J
R
i
0
(5)
where vel (x, y, t ) is the velocity in the point (x, y ) (radius r ) at time t , in the
interior of a cylinder of length L and radius R ; is the blood density, is the viscosity
1819
Fig. 1. Analytic Womersley model. (a) The pressure difference which is the input of our model. (b) and (c) the mean velocity and WSS obtained by the Womersley model.
(d) The ow solution. (e) We observe four velocity proles at different times (0.077 s, 0.205 s, 0.256 s, and 0.333 s for the cardiac phases 3, 9, 11, and 14 respectively) and the
2D triangular mesh.
and v = / is the kinematic viscosity. A0 is the mean value of the pressure gradient
PGm (t ) . J is the Bessel function of the rst kind and order . The parameter
= R /v is a non-dimensional parameter known as the Womersley number, with
frequency .
For obtaining physiological peak ow and velocities similar to those in the
normal aorta, but not necessarily physiological waveform along time, we considered a cylinder of length 10 cm, diameter 2 cm, with a pressure gradient range
7 6.4 mm Hg, 40 cardiac phases and a heart rate of 60 beats per minutes. These
values yielded a time average (average along the time) of mean velocity equal to
45.29 cm/s, mean ow equal to 141.3 ml/s. The WSS can be obtained by
differentiating Eq. (5) at the vessel wall, as shown in Eq. (6). Using this equation we
obtained a time average of axial WSS of 0.85 N/m2.
(R , t ) =
PGm (t ) R
A0 R
+ Re
2
i
3/2
i
v
J1 R
J R
0
(
(
)
)
3/2
i
v
3/2
i
v
(6)
1820
Fig. 2. (a) The seven different mesh resolutions used for the Womersley analysis. (b) Three different Gaussian noise levels with mean 0 and standard deviation of 0.25%, 0.5%
and 1% of the peak velocity value that was 1.65 m/s; the velocity prole corresponds to cardiac phase number 11 at time 0.256 s. (c,d) The procedure for assessing the effect
of an incorrect position of the segmentation in the analysis of WSS: (c) erosion and (d) dilatation.
1821
Fig. 3. (a) Schematic illustration of the location of analyzed planes. These planes were positioned in the ascending aorta (AO1), at the beginning and the end of aortic arch
(AO2AO3) and at the descending aorta (AO4AO5), with the innermost curvature reference positions marked by dots. (b) The mesh generation process. From the 2D PC-MRI
we draw a region of interest (ROI) in the T1 magnitude image (anatomical); in this case the ROI was drawn in section AO1. The vessel lumen of the region was then
segmented using a ChanVese algorithm; subsequently, each node (pixel in the 2D image) of the domain of interest was identied, and the triangular mesh was generated.
smoothing lters were applied to the 2D CINE PC-MRI datasets before the segmentation process. The nite-element mesh was generated by creating triangular
elements, where each node of the mesh was located in the center of pixels in the
segmented region, covering the entire lumen (Fig. 3b).
3.2.2. Effects of MRI resolution
An experiment similar to the one performed in the Womersley model was
carried out in vivo. In one volunteer we acquired ve datasets with different
resolutions at the AO1 level, 0.7 0.7 mm, 1.0 1.0 mm, 1.25 1.25 mm,
1.5 1.5 mm and 2.0 2.0 mm. Additionally, for each dataset of this volunteer the
WSS values were obtained using ve different element sizes with an element area
of 0.49 mm2, 1 mm2, 1.56 mm2, 2.25 mm2 and 4.0 mm2. We analyzed the WSS
values only in the systolic phase. When the center of the element did not match the
pixel center the velocity data were interpolated using a cubic interpolation.
Table 1
WSS contour mean and standard deviation, for the cardiac phases (13, 16, 29) and
different element sizes.
ES
(T*)
N1
N2
N3
N4
CP13
0.01
0.05
0.1
0.5
1.0
1.5
2.0
7.40
7.40
7.40
7.40
7.40
7.40
7.40
6.8 70.09
6.3 70.18
5.8 70.25
4.0 70.52
3.1 70.45
2.5 70.54
1.8 70.44
6.8 70.18
6.3 70.20
5.8 70.26
4.0 70.52
3.1 70.45
2.5 70.54
1.8 70.45
6.8 70.34
6.2 70.24
5.8 70.28
4.0 70.54
3.1 70.44
2.5 70.55
1.8 70.44
6.8 7 0.65
6.3 7 0.40
5.8 7 0.29
4.0 7 0.53
3.17 0.47
2.5 7 0.52
1.8 7 0.47
CP16
0.01
0.05
0.1
0.5
1.0
1.5
2.0
5.82
5.82
5.82
5.82
5.82
5.82
5.82
5.7 70.02
5.5 70.07
5.4 70.11
4.3 70.36
3.7 70.37
3.2 70.47
2.6 70.43
5.7 70.10
5.5 70.10
5.4 70.11
4.3 70.36
3.7 70.38
3.2 70.47
2.6 70.43
5.6 70.63
5.5 70.31
5.4 70.24
4.3 70.38
3.7 70.41
3.2 70.48
2.6 70.42
5.6 7 0.63
5.5 7 0.31
5.4 7 0.24
4.3 7 0.38
3.7 7 0.41
3.2 7 0.48
2.6 7 0.43
CP29
0.01
0.05
0.1
0.5
1.0
1.5
2.0
5.48
5.48
5.48
5.48
5.48
5.48
5.48
5.2 70.04
4.9 70.09
4.7 70.13
3.7 70.30
3.2 70.27
2.8 70.34
2.4 70.29
5.2 70.37
4.9 70.16
4.7 70.17
3.7 70.28
3.2 70.28
2.8 70.33
2.4 70.30
5.2 7 0.68
4.9 7 0.33
4.7 7 0.23
3.7 7 0.31
3.2 7 0.28
2.8 7 0.33
2.4 7 0.30
WSS =
C t w dL
C
WSS =
tw
2
WSS d L ,
(7)
MeanD =
N
a
b
cp
=1 t cp t cp
),
5.2 70.12
4.9 70.12
4.7 70.15
3.7 70.31
3.2 70.27
2.8 7 0.34
2.4 70.29
(8)
b
a
where tcp
is the WSS contour mean value processed by one observer a and tcp
is the equivalent value processed by the other observer b , for each cardiac phase
(cp 1,..,40).
4. Results
4.1. Robustness analysis
In Table 1 we show the results of the axial WSS contour mean
(WSS ) and standard deviation (WSS ) for three representative
cardiac phases. We selected two phases that showed a peak forward and backward ow (Fig. 4a), and one cardiac phase that
showed a peak in WSS, as indicated in Fig. 4b. In our simulation
these values corresponded to the times of 0.307 s (cardiac phase
13, peak WSS), 0.384 s (cardiac phase 16, peak retrograde ow)
and 0.717 s (cardiac phase 29, peak forward ow). As observed in
Table 1, the WSS values obtained with our method were similar to
the theoretical ones for the smallest elements. Notably, our results
also show that the levels of noise had a negligible effect on the
results for any cardiac phase.
1822
Fig. 4. (a) Flow and (b) WSS contour mean as function of time for different element sizes. The analytic values are shown in black; we observed that as the element mesh size
is smaller the ow and WSS contour mean value converge to the theoretical one. (c) Different velocity proles for cardiac phases 13, 16 and 29, at time 0.307 s, 0.384 s and
0.717 s respectively.
1823
Fig. 5. Resulting WSS for different positions of the vessel wall for cardiac phase 13. The rst row shows the WSS obtained when the segmentation curve is placed correctly at
the vessel wall. The second row shows the WSS obtained when the segmentation curve is erroneously moved outwards by 0.5 mm. The third row shows the corresponding
results when the segmentation curve is erroneously moved inwards by 0.5 mm. The columns show seven different spatial resolutions of the mesh.
5. Discussion
We have proposed a novel approach for the determination of
WSS distributions using nite-element and stress-recovery
methods based on 2D cine PC-MRI. The proposed method has
distinctive theoretical advantages. First, the nite-element
approach allows for effortless and automatic-meshing procedures
based on segmented images. Second, it delivers an estimate of the
shear stress, or any spatial derivative of the velocity eld, that
converges to the exact solution as the element size of the mesh
decreases, as shown for the case of the Womersley model. This
trend is consistent with the well-known convergence properties of
nite-element approximations (Zienkiewicz et al., 2005). Third,
the proposed method delivers a continuous eld for the shear
stress tensor inside the lumen of the vessel under analysis.
1824
Fig. 6. Time average ow and WSS contour means, for different element size subjected to changes of position of the vessel wall (dilation and erosion). The theoretical value
(TV) of ow volume and time average of WSS contour mean values were 141.3 ml/s and 0.85 N/m2, respectively. D1, displacement of 0 mm; D2, displacement of 0.5 mm; D3,
displacement of 1 mm; D4, displacement of 2 mm.
1825
Fig. 7. Plots of the ow, WSS axial (WSS Axi.), WSS circumferential (WSS Cir.) and WSS magnitude (WSS Mag.) for the sections AO1 (a), AO3 (b) and AO5 (c). Additionally,
(d) shows the time average and standard deviation (in parentheses) between volunteers of different variables for each section.
1826
Table 2
Inter-observer and intra-observer analysis for volunteer data. We show the mean absolute error and standard deviation ( 7 ) between observers for the ow, area, mean
velocity, time to peak. Additionally, we show the mean absolute error and standard deviation for the time average of axial (Axi.), circumferential (Cir.), and magnitude (Mag.)
of WSS.
AO1
AO2
AO3
AO4
AO5
Inter-observer
Flow (ml/s)
Area (mm2)
Mean velocity (m/s)
Time to peak (ms)
Mean diff Axi. WSS (N/m2)
Mean diff Cir. WSS (N/m2)
Mean diff Mag. WSS (N/m2)
2.17 1.4
16.5 7 5.2
0.7 7 0.4
0.0 7 0.0
0.0277 0.046
0.0137 0.015
0.029 7 0.047
1.4 70.5
11.9 74.4
0.6 70.4
0.0 70.0
0.029 70.043
0.014 70.014
0.030 70.044
2.17 1.6
10.7 7 9.5
1.2 7 0.6
0.0 7 0.0
0.0377 0.054
0.0117 0.009
0.036 7 0.053
0.9 7 0.6
5.2 7 2.5
0.5 7 0.2
0.0 7 0.0
0.0217 0.031
0.0077 0.009
0.022 7 0.030
1.0 7 1.0
6.17 5.5
1.0 7 0.6
0.0 7 0.0
0.0467 0.062
0.0127 0.013
0.0407 0.063
Intra-observer
Flow (ml/s)
Area (mm2)
Mean velocity (m/s)
Time to peak (ms)
Mean diff Axi. WSS (N/m2)
Mean diff Cir. WSS (N/m2)
Mean diff Mag. WSS (N/m2)
2.6 7 2.1
23.7 7 10.4
0.7 7 0.3
0.0 7 0.0
0.0277 0.044
0.0097 0.011
0.028 7 0.044
1.9 71.0
16.1 77.4
0.9 70.4
0.0 70.0
0.020 70.030
0.009 70.011
0.020 70.032
2.8 7 1.6
15.17 7.6
1.2 7 0.7
0.0 7 0.0
0.026 7 0.043
0.0097 0.009
0.026 7 0.041
1.2 7 1.4
7.4 7 8.1
0.6 7 0.5
0.0 7 0.0
0.0197 0.030
0.0077 0.008
0.0197 0.029
1.3 7 0.8
9.9 7 5.3
1.17 0.2
0.0 7 0.0
0.034 7 0.051
0.0077 0.009
0.032 7 0.052
Table 3
Axial (Axi.), circumferential (Cir.) and magnitude (Mag.) of WSS contour mean, for
the systolic phase of the data acquired in one volunteer with different resolutions
and analyzed with different element sizes. For this experiment, we select as a
reference the WSS value obtained with spatial resolution of 0.7x0.7 mm and element size of 0.49 mm2. These values are marked with * in the table.
MRI resolution (mm)
0.7 0.7 1.0 1.0 1.25 1.25 1.5 1.5 2.0 2.0
Element
size
(mm2)
WSS
Axi.
WSS
Cir.
WSS
Mag.
0.49
1.00
1.56
2.25
4.00
1.33*
1.11
1.04
0.93
0.81
1.59
1.30
1.13
1.01
0.85
1.63
1.28
1.15
1.03
0.82
1.50
1.21
1.01
0.94
0.78
1.55
1.21
1.01
0.88
0.75
0.49
1.00
1.56
2.25
4.00
0.09*
0.05
0.04
0.04
0.04
0.11
0.06
0.05
0.04
0.04
0.09
0.06
0.05
0.05
0.05
0.07
0.04
0.04
0.04
0.04
0.08
0.04
0.03
0.02
0.02
0.49
1.00
1.56
2.25
4.00
1.34*
1.11
1.05
0.93
0.81
1.59
1.30
1.13
1.01
0.85
1.64
1.28
1.15
1.03
0.82
1.50
1.21
1.01
0.94
0.78
1.55
1.22
1.01
0.88
0.75
Acknowledgment
The authors acknowledge the support of the Interdisciplinary
Research Fund VRI# 44/2011 from the Ponticia Universidad
Catlica de Chile, Anillo ACT 079, and FONDECYT through Grants
#11100427, #11121224 and #1141036. Julio Sotelo thanks CONICYT
and the Ministry of Education of Chile, with his higher education
program, for the graduate scholarship for doctoral studies.
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