A Computational Study of Perfusion During The ExtraCorporeal Membrane Oxygenation (ECMO)

International Journal of Privacy and Health Information Management
Volume 5 • Issue 1 • January-June 2017
A Computational Study of Perfusion

During the ExtraCorporeal
Membrane Oxygenation (ECMO)
Maria Vittoria Caruso, Bioengineering Unit, University Magna Grecia of Catanzaro, Catanzaro, Italy
Vera Gramigna, Bioengineering Unit, University Magna Graecia of Catanzaro, Catanzaro, Italy
Attilio Renzulli, Cardiac Surgery Unit, University Magna Graecia of Catanzaro, Catanzaro, Italy
Gionata Fragomeni, Bioengineering Unit, University Magna Graecia of Catanzaro, Catanzaro, Italy
ABSTRACT
The extracorporeal membrane oxygenation (ECMO) is a common procedure of extracorporeal

circulation (ECC) used in case of cardiopulmonary diseases. The major clinical complications are
related to hemodynamic changes and to the mechanical shear stress. The aim of this study is to
evaluate the effects of the modality of perfusion during ECMO, comparing the hemodynamic behavior
generated by constant flow (normal modality) with the one obtained by pulsed perfusion induced by
the intra-aortic balloon pump (IABP). To carry out the study, the computational fluid dynamic (CFD)
approach was chosen, realizing a multi-scale model. The numerical results have highlighted that the
IABP-induced pulsed perfusion increases both flow and pressure in the supraaortic vessels, even if
the balloon makes the wall shear stress (WSS) pattern and the hemolysis index worse.
Keywords
Computational Fluid Dynamics (CFD), ExtraCorporeal Membrane Oxygenation (ECMO), Hemodynamics,
Hemolysis, Intra-Aortic Balloon Pump (IABP), Wall Shear Stress (WSS)
INTRODUCTION
The extracorporeal membrane oxygenation (ECMO) is an extracorporeal procedure used for patients
with cardiac or respiratory failures who do not react to conventional therapy (Harry Anderson, 1993;
Paolini, 1994; Smith, 2001). Furthermore, it is also adopted as a post-operative circulation support after
cardiac surgeries and as a prolonged but temporary support for weaning from the cardiopulmonary
bypass (CPB) (Doll, 2004). The main clinical complications of the ECMO-treated patients are
cerebral injuries and infarction, which can cause death (Doll, 2004; Risnes, 2005). Indeed, hemolysis,
thromboembolic events and internal blending are the major complications related to the artificial organs
(Goubergrits, 2006), and, above all, to the mechanical shear stress. To overcome them, anticoagulants
must be administered even if they worsen the performance of the devices (Goubergrits, 2004).
As reported in (Ji, 2006), the pulsed perfusion during the extracorporeal circulation is healthier
compared to the normal one, that is characterized by constant/linear flow. In 1977 the intra-aortic
DOI: 10.4018/IJPHIM.2017010103
Copyright © 2017, IGI Global. Copying or distributing in print or electronic forms without written permission of IGI Global is prohibited.
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balloon pump (IABP) was proposed by (Bregman, 1977) as a useful device to provide pulsatile flow
during CPB. The principal component of this mechanical support is a polyethylene balloon placed
in the aorta after the left subclavian artery and before the iliac bifurcation, which inflates/deflates
according to the cardiac cycle or setting the assistance level when there is no heart activity, such as
during CPB or ECMO. Recently, some studies have highlighted different benefits of IABP-induced
pulsatility during ECMO (Madershahian, 2009; Madershahian, 2011; Petroni, 2014; Yang, 2014).
Based to our knowledge, there is little information regarding the hemodynamic pattern in aorta
and its incidence on clinical complications and, so, on illness development during normal/constant
ECMO and IABP-induced pulsed ECMO. Therefore, a detailed analysis is necessary.
The purpose of this study is to investigate the hemodynamic changes in aorta and in the epiaortic
vessels during ECMO assistance by comparing the two modalities of perfusion. Furthermore, the
wall shear stress (WSS) and the hemolysis index patterns were evaluated in order to identify the
typology of more susceptible perfusion in the clinical complication onset. The computational fluid
dynamic (CFD) approach was chosen to carry out the analysis because it represents a valid, practical
and efficient tool that allows to investigate the hemodynamics through the resolution of numerical
simulations (Tu, 2007). In addition, a multi-scale model (Quarteroni, 2003) was developed in order
to specify the boundary conditions.
MATERIALS AND METHODS
Geometrical Models
To analyze the hemodynamics in the aorta and in the epiaortic vessels during normal and pulsed
perfusion in ECMO, a healthy aorta model was reconstructed starting from Dicom images sequence
obtained from CT of a 54-year-old man, done for clinical reasons. Informed written consent was
obtained from the patient to use medical images. The anatomy of the aorta was modeled using Itk-
Snap, an open source segmentation software. Since it provides a stereolithographic’s file (stl format),
the 3D aorta surface was converted in 3D solid model by means of the reverse engineering process.
The aorta geometry included the ascending aorta, the aortic arch with its three epiaortic vessels
(brachiocephalic artery, left carotid artery, left subclavian artery) and the descending aorta (Figure 1).
A standard ECMO arterial cannula (24 Fr Medtronic Inc., Minneapolis, MN, USA) was modeled
and it was placed in the ascending aorta on the site that is routinely adopted at our institution: 2 cm
below the take-off of the brachiocephalic artery on the anterior wall of the vessel, with a tilt angle
of 45° respect to the transversal plane (Figure 1).
The intra-aortic balloon (IAB) was modeled considering a volume of 40 cm3 (Sensation 7 Fr
40 cm3 and CS300 IABP System, Datascope, Maquet GmbH and Co. KG, Rastatt, Germany) and
ignoring the conical terminal parts.
Since the aim of the study was the investigation of aortic hemodynamics during two different
types of perfusion during ECMO, two geometrical models were considered:
• Normal Perfusion: In this case the model included the aorta and the ECMO cannula;
• Pulsed Perfusion: In this case the model included the aorta, the ECMO cannula and the IAB.
Mathematical Model
From a macroscopic point of view, the blood has a density of 1,060 kg/m3 (Cutnell, 1998) and a
non-Newtonian behavior, but for large vessels it can be modeled as an incompressible and Newtonian
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Figure 1. Multi-scale model, obtained coupling the 3D aorta model and the resistance 0D model, of pulsed case (left) and IAB
radius change behavior (right)
fluid (Formaggia, 2009), with viscosity of 0.0035 Pa∙s (Yilmaz, 2008). Its motion is described by
means of the 3D Navier-Stokes equations:
∇⋅u = 0 (1)
 T
ρ (∂u / ∂t ) + ρ (u ⋅ ∇) u = ∇ ⋅ [−p I + µ ∇u + (∇u)  + F (2)
 
where u represents the fluid velocity vector, p the pressure, µ the dynamic viscosity, ρ the density of
blood, I the identity matrix and F the volume force field, which was neglected in the computational
study because the effect of gravity was ignored (the patient was supine during the surgical procedure).
The laminar flow was hypothesized because, considering the inlet flow (see next section), Reynolds
number was about 3,400 in ECMO cannula and about 1,200 in ascending aorta.
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Since during ECMO there is no heart activity, an assistance level of 70 bpm was hypothesized and
the balloon change behavior was approximated with an 8 degree Fourier general model: the balloon
inflation starts at 0.2 s and the maximum volume is reached in 0.25 s, considering a cardiac cycle of
about 1 s, so a “false” systolic peak, due to IABP, occurs at 0.45 sec (Figure 1).
To evaluate the stress due to the blood motion on a specific vessel, the wall shear stress (WSS)
can be evaluated, according to the following equation:
+ (τy ) + (τz )
2
(τ )
2 2
WSS = x
(3)
where τx, τy and τz were the viscous stress in the x, y and z directions, respectively. WSS, generally
expressed in [Pa], is a time-dependent indicator correlated to the atherosclerosis (Malek, 1999).
The blood damage is due to the interaction with mechanical parts, known as hemolysis, that
frees hemoglobin in the plasma, dangerous for the organism (Garon, 2004; Taskin, 2012). Generally
Lagrangian approach is used to describe this phenomenon (Goubergrits, 2004; Taskin, 2012), but for
complex computational domains, Eulerian approach is preferred (Garon, 2004), according to which
the hemolysis index can be evaluated as a power law:
HI =a 1/b ⋅ τ c /b (4)
where a, b and c are constants (Giersiepen, 1990) and τ is the scalar shear stress, evaluated starting
from the tensor by means of Von Mises criterion (Garon, 2004; Taskin, 2012).
Boundary Conditions
As in clinical practice, in this study the total flow was delivered through the ECMO cannula, so
the ascending aorta was considered as clamped (no cardiac output came from the heart). As inlet
boundary condition, a constant flow of 5.5 l/min was applied, whereas the lumped parameter model
was chosen to represent the downstream domain. For this reason, a multi-scale model (Quarteroni,
2003) 3D-0D was implemented. As lumped parameter model, the resistance was adopted to specify
the relationship between flow and pressure, as in other studies (Bazilevs, 2009; Caruso, 2015;
De Zelicourt, 2012; Vignon-Clementel, 2010; Yang, 2010). Resistances at the four outflow exits
(brachiocephalic artery, left common carotid artery, left subclavian artery and descending aorta)
were imposed by the following pressure equation:
p = p0 + R ⋅ Q (5)
where p0 is an outlet pressure offset, Q indicates the instantaneous volumetric flow rate through each
respective outflow exits, calculated at each instant from the local velocity profile, and R the resistance.
Furthermore, p0 was evaluated to ensure the mean arterial pressure (MAP) maintained during ECMO
support (MAP > 70 mmHg) (Doll, 2004). Considering that the blood demand depends on the needs of
organs and tissues (Caruso, 2015), it has been hypothesized that the flow rate percentages, correlated
to the resistance value, remain the same in ECMO support independently of the modality of perfusion.
Moreover, even if the arterial walls are elastic, in this study the vessel and the arterial cannula
walls were approximated to be rigid and no-slip boundary conditions were applied, because the
aim of this study was to investigate only the effects of IABP during ECMO support. Moreover, this
simplification was also assumed in order to reduce the computational cost that was very high when
the IABP inflation was numerically reproduced.
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Simulation Details
The computational analysis was carried out using COMSOL 5.0 (COMSOL Inc, Stockholm, Sweden),
a finite-element-based commercial software package. Since two different geometrical models were
necessary to compare the normal and the pulsed perfusions in ECMO, two simulations were carried out:
• Normal Perfusion: In this case a time-dependent study was performed, using the direct
solver Pardiso, the BDF method the time stepping and linear formulation for both the velocity
components and the pressure field (P1+P1); the mesh consists of 101,264 tetrahedral elements;
• Pulsed Perfusion: In this case a parametric study was performed, reproducing a “false” transitory
study, using the direct solver Pardiso and linear formulation (P1+P1); the mesh consists of
376,796 tetrahedral elements.
The mesh size was different because, during the normal perfusion, the geometrical model consisted
only of the aorta anatomy and the arterial cannula, whereas in the assisted one there was also the
balloon in the descending aorta. Furthermore, these two meshes were chosen in order to obtain a
good quality, a content computational cost and accurate solutions. Considering the continuity law,
the grid error can be expressed as:
Qin − CTF
e= ⋅100 (6)
Qin
where Qin is the flow imposed as inlet boundary condition and CTF is the calculated total flow,
expressed as:
CTF = ∑qi (7)

i =0
in which i indicates the branch (0: asc. aorta, 1: brachioc. art., .... 4: desc. aorta).
The mesh used generated an absolute error of less than the 5% - 2.9% in case of normal perfusion
and 3.8% in case of pulsed one -, an acceptable error to consider the solution as grid independent.
For both simulations, four cycles, with a step of 0.001, were considered to eliminate the transitory
initial effects due to the converge process of CFD analysis and to guarantee stable solutions. The last
cycle (3- 4 s) was investigated.
RESULTS
In Figure 2 the flow waveforms over one cardiac cycle (3- 4 s) are illustrated. Obviously, in case of
normal perfusion (Figure 2A), all flows present constant values over time; instead, in case of pulsed
perfusion (Figure 2B), the flow follows the IAB radius change behavior: the supraaortic vessels present
the same trend, while the descending aorta is characterized by the opposite trend due to the presence
of the balloon that occludes this trunk, so the flow decreases. Furthermore, the flow waveforms are
comparable for the left carotid and the left subclavian arteries in both modalities of perfusion.
A similar situation is obtained for the pressure waveforms (Figure 3).
In Table 1 the mean flow and the mean pressure, evaluated in one cardiac cycle (3- 4 s), are
summarized. The presence of IAB increases both the hemodynamic variables in supraaortic vessels,
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Figure 2. Flow distributions over a cardiac cycle for each vessel in case of normal perfusion (A) and of pulsed one (B)
Figure 3. Pressure distributions over a cardiac cycle for each vessel in case of normal perfusion (A) and of pulsed one (B)
Table 1. Mean flow and mean pressure for each vessel in case of normal perfusion (NP) and of pulsed perfusion (PP). D:
difference between NP and PP, evaluated with Equation (8)
Flow Pressure
Mean Flow [l/min] Mean Pressure [mmHg]
Vessel [%] [%]
NP PP D NP PP D
Asc. Aorta 0.00 0.00 0.00 74.13 77.44 4.47
Brachioc. A. 0.80 0.90 12.50 73.95 77.23 4.44
Left Carotid A. 0.39 0.44 12.82 74.45 77.86 4.58
Left Subc. A. 0.40 0.45 12.50 74.85 78.41 4.76
Desc. Aorta 4.07 3.92 -3.68 73.48 72.35 -1.54
45
whereas the descending aorta is characterized by a decrease of flow and pressure. Furthermore,
evaluating the difference (D) as:
NP − PP
D= ⋅100 (8)
NP
the flow and the pressure in the supraaortic vessels increase in case of pulsed perfusion (PP) of about
12.5% and of about 4.5% respect to the normal perfusion (NP).
To better analyze the effects of the two modalities of perfusion, the streamlines of the velocity
magnitude are reported in Figure 4. Both in normal and in pulsed cases, the ascending aorta is
characterized by high swirling flow and stagnation zones. In presence of balloon (Figure 4 B1 and
B2) a chaotic behavior occurs in the aortic arch below the brachiocephalic artery, with high velocity.
Furthermore, when the IAB is inflated (Figure 4 B2), the clogged descending aorta generates a
recirculation flow in the aortic arch.
The velocity pattern in correspondence of the emergence of the epiaortic vessels (Figure 5)
shows that the highest velocity value occurs in different points comparing the normal perfusion and
Figure 4. Stremlines of velocity magnitude in case of normal perfusion (A) and of pulsed one (B), considering the deflation instant
(IABP-off, B1) and the inflation instant (IABP-on, B2)
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Figure 5. Height pattern of velocity magnitude in a cutplane below the supraaortic vessel in case of normal perfusion (A) and of
pulsed one (B), considering the deflation instant (IABP-off, B1) and the inflation instant (IABP-on, B2)
the pulsed one, considering also the deflated and the inflated IABP. In case of constant flow (Figure
5A), the maximum value is recorded in correspondence of the left subclavian artery; in case of pulsed
perfusion, when the balloon is closed (Figure 5 B1), the left subclavian artery and the left carotid artery
present similar values, whereas the last one has the higher velocity when the IAB is on (Figure 5 B2).
Finally, the WSS and the HI percentage patterns (Figure 6) illustrate that the pulsed perfusion
increases the stress in correspondence of the emergence of the epiaortic vessels and decreases it in
the descending aorta and that the highest blood damage occurs at the entrance of left carotid and
Figure 6. Wall shear stress (WSS) and hemolysis index (HI%) in case of normal perfusion (A) and of pulsed one, considering the
inflation instant (IABP-on, B2)
47
left subclavian arteries. Furthermore, the value of HI percentage evaluated on the internal curvature
of aortic arch is lower in case of counterpulsation when the balloon is inflated (6.25% in constant
perfusion compared to 5.85% in pulsed one).
DISCUSSION
The ECMO is a medical procedure used in case of cardio-respiratory failures that perfuses the
organism with constant flow. Since some studies have presented different advantages of IABP-induced
pulsatility during ECMO (Madershahian, 2009; Madershahian, 2011; Petroni, 2014; Yang, 2014) and
since little information is available regarding the hemodynamics and its correlation with some clinical
complications in case of normal and pulsed perfusion in ECMO, this study was carried out in order
to compare these two modalities of perfusion. To solve the analysis, the computational approach was
used, in which the balloon inflation was numerically reproduced by means of a parametric study.
Furthermore, the multi-scale methodology (Quarteroni, 2003) was chosen to model the problem,
coupling the 3D model of aorta with a 0D-resistance model, whose values were evaluated in order
to maintain the MAP greater than 70 mmHg in case of both normal and in pulsed perfusions, as in
clinical practice (Doll, 2004).
The numerical results of this study demonstrated that the type of perfusion has significant
effects on hemodynamics in the aorta and, as a consequence, on WSS and hemolysis, two of the
most important parameters correlated with some illnesses (Malek, 1999; Garon, 2004; Taskin, 2012).
Since the resistance model was applied as outlet boundary condition in both perfusion types, the
pressure and the flow present the same behavior over the cardiac cycle: during the normal perfusion
they have constant values, whereas in pulsed modality they follow the balloon radius change over the
cardiac cycle. In addition, the IABP increases the flow rate in the supraaortic vessels of about 12.5%
in respect to the linear perfusion, but increases the stagnation flow and stasis in the descending aorta.
Also, the pressure increases of about 4.5% in the supraaortic vessels during the pulsed perfusion,
whereas it decreases in the descending aorta. Indeed, the balloon inflation causes a blood volume
displacement within the aorta, generating an increase in flow and pressure distribution in the proximal
vessels, as reported in (Krishna, 2009). Furthermore, since brain hypoperfusion might be the primary
cause of different injuries including stroke, encephalopathy and cognitive dysfunctions (Hogue, 2006),
the pulsed perfusion ensures a healthier hemodynamic profile.
Regarding the WSS, as expected, it is high in the ECMO cannula and it is lower in the aorta due
to the different diameter of the two vessels (small diameter of the cannula in respect to the caliber of
the ascending aorta). Furthermore, the aortic walls opposite to the jet of cannula present high values
due to the impact of perfusion flow. These situations are in agreement with (May-Newman, 2006;
Caruso, 2015). In case of pulsed perfusion, the emergence of left carotid artery is the best stressed,
with a value of about 3 Pa, so atheroprotective phenotype is stimulated (Malek, 1999). Moreover, since
atherogenesis plaques preferentially involve the regions characterized by chaotic flow pattern, stasis
and low WSS (Malek, 1999), in case of pulsed perfusion the descending aorta is more vulnerable to
the atherosclerosis events.
Analyzing the hemolysis index percentage, in case of constant flow a greater blood damage
occurs in correspondence of the aortic walls opposite the jet of cannula (6.25% compared to 5.85%),
even if the damage at the entrance of the left carotid artery increases in pulsed perfusion. Indeed, in
presence of balloon, the hematocrit often decreases due to hemolysis from mechanical damage to
the red blood cells (Krishna, 2009).
Although this study gives information about the hemodynamics during ECMO, it presents several
limitations, as reported in the methodology.
First, since the difference between the Newtonian model and the non-Newtonian one is negligible
for large vessels as the aorta (Formaggia, 2009), in this study the first model was adopted to describe
fluid behavior. Second, the aortic wall compliance was ignored in order to investigate only the IABP
48
influence on hemodynamics during ECMO and to reduce the computational cost that was very high
when the IABP inflation was numerically reproduced by means of a parametric study.
Finally, the comparison was made by hypothesizing that resistances values remain the same in
presence of counterpulsation because it was assumed that the blood demand depends on the needs
of organs and tissues (Caruso, 2015), so the percentages flow rate, correlated to the resistance value,
remain the same in ECMO support independently of the modality of perfusion.
In order to improve this computational comparison, further improvements will be addressed
implementing a non-Newtonian behavior for the blood rheology, a fluid-structure model that,
using results from ex-vivo tensile tests on aortic tissues, takes into account the contribution of wall
deformation and evaluating in-vivo the resistance during pulsed perfusion.
CONCLUSION
In case of cardio-pulmonary failure, the extracorporeal membrane oxygenation can be used as

mechanical circulatory support. Its perfusion is generally constant over the cardiac cycle, but a
pulsatile flow can be obtained using the intra-aortic balloon pump.
This computational study was carried out in order to investigate the hemodynamics in the
aorta by comparing these two modalities of perfusion, analyzing also the incidence on clinical
complications by means of the evaluation of two mechanical indicators, namely the wall shear stress
and the hemolysis index.
The numerical results have highlighted the benefits and the disadvantages of the pulsed perfusion.
Indeed, although the flow and the pressure field increase in the supraaortic vessels, thus reducing
brain hypoperfusion, atherosclerosis events have eased and the blood damage increases.
49
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left ventricular assist devices on hemodynamics of a pediatric end-to-side anastomotic graft. Cardiovascular
engineering and technology, 1(1), 88-103.
Yilmaz, F., & Gundogdu, M. Y. (2008). A critical review on blood flow in large arteries; relevance to blood
rheology, viscosity models, and physiologic conditions. Korea-Australia Rheology Journal, 20(4), 197–211.
51
Maria Vittoria Caruso graduated in Mechanical Engineering at the University of Calabria in 2011. She received the
PhD in Biomedical and Computer Engineering at Magna Graecia University of Catanzaro in 2015. Her research
interests include computational fluid dynamics (CFD), multiscale modeling, hemodynamics, mechanical assistance
of the cardiovascular system, numerical modeling of cardiovascular system.
Vera Gramigna graduated in Mechanical Engineering at the University of Calabria in 2007. She received PhD in
Biomedical and Computer Engineering at University Magna Graecia of Catanzaro in 2011. Her main research
area is focused on application of computational fluid dynamic models and numerical approach to cardiovascular
system in physiological condition and in presence of diseases.
Attilio Renzulli graduated in Medicine and Surgery at the University of Naples in 1979, specialized in Cardiovascular
Surgery in 1984 and in thoracic surgery in 1989. He received the PhD in Medical Surgical Pathophysiology of the
Cardiothoracic and Respiratory Apparatus and Associate Biotechnologies in 2003. He is a Professor at the Faculty
of Medicine at Magna Graecia University of Catanzaro. His main topics of research are: adult cardiac surgery,
heart valve surgery, arrhythmias surgery, extracorporeal circulation, mechanical assistance.
Gionata Fragomeni graduated in Engineering at the University of Calabria in 1997. He received the PhD in
Bioengineering from the University of Bologna in 2003. He was a temporary chair in Cardiovascular Mechanics
and Mechanics for Biomedical Applications at Calabria University and Magna Graecia University. He is an Assistant
Professor at the Faculty of Medicine at Magna Graecia University of Catanzaro. Prof. Gionata Fragomeni was the
coordinator of two national research projects financed by the Italian Ministry of Research, and has authored over
100 publications on journals and international conference proceedings. His research interests include Bio-Fluid
Dynamics, Computer Modeling and Cardiovascular Mechanics.
52

A Computational Study of Perfusion During The ExtraCorporeal Membrane Oxygenation (ECMO)

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Volume 5 • Issue 1 • January-June 2017