Impact of Pericardial Effusion on Cardiac Mechanics in Patients

with Dilated Cardiomyopathy

Francesco Scardulla

, Antonino Rinaudo

, Cesare Scardulla

and Salvatore Pasta

Dipartimento di Ingegneria Chimica, Gestionale, Informatica e Meccanica, Universita' di Palermo,

Viale delle Scienze Ed. 8, 90128 Palermo, Italy

Mediterranean Institute for Transplantation and Advanced Specialized Therapies (ISMETT),

Via Tricomi n.1, 90127, Palermo, Italy

Fondazione RiMED, Via Bandiera n.11, 90133, Palermo, Italy

Keywords: Finite Element Analysis, Cardiac Mechanics, Cardiomyopathy, Pericardial Effusion.

Abstract: Dilated cardiomyopathy (CDM) is a degenerative disease of the myocardium accompanied by left

ventricular (LV) remodeling, resulting in an impaired pump performance. Differently, pericardial effusion

(PE) is a liquid accumulation in the pericardial cavity, which may inhibit blood filling of heart chambers.

Clinical evidence show that PE may improve pump performance in patients with CDM. Therefore, this

study aims to assess wall stress and global function of patients with CDM, PE as compared to healthy

patient. These findings suggests that CDM has an important implication in the mechanical changes of LV

and right ventricle by increasing wall stress and reducing pump function. Conversely, PE determines

lowering myocardial fiber stress and improves global function as compared to those of CDM.

1 INTRODUCTION

Dilated cardiomyopathy (CDM) is a degenerative

disease of the myocardial tissue accompanied by left

ventricular (LV) remodeling (Nakayama et al.,

1987). The histologic characteristics of CDM

include hypertrophy of myofibers, myofibrillar lysis,

nuclear changes and vacuolization of myocardial

fibers and interstitial fibrosis of the myocardium

(Hayashida et al., 1990). LV remodeling is a

multistep process that involves acute dilation of the

infarcted area, increase of LV volume, lengthening

of the LV perimeter, and decrease of LV curvature.

Natural history studies show that progressive LV

remodeling is directly related to future deterioration

of LV performance and a poor clinical course (Cohn

et al., 2000) (Swynghedauw, 1999).

Pericardial effusion (PE) is a pathological

accumulation of ﬂuid within the pericardial space

(Mirhosseini et al., 2013). Usually, such disease do

not inﬂuence clinical decision-making as long as the

PE is not considered haemodynamically

compromising cardiac functionality (Frohlich et al.,

2013). PE ﬂuid accumulation can be attributed to an

underlying systemic or local inﬂammatory process

such as cancer or myo-/pericarditis or might occur

after surgery or can be secondary to congestive,

severe heart failure. However, the mechanism of PE

development and its prognostic value in heart

failure remain elusive. A persistent PE at

echocardiographic follow-up was associated with

unfavourable outcome when compared with patients

with resolved PE. Indeed, patients with PE exhibit

worse right ventricular (RV) function, larger right

atrial dimensions, more pronounced tricuspid

regurgitation as well as a higher prevalence of

pulmonary hypertension. A recent study shows that

patients with PE have signiﬁcantly elevated RA

ﬁlling pressures and an increased mean arterial

pulmonary pressure, whereas the left ventricular

ﬁlling pressure and wedge pressure did not differ

between PE and control group (Frohlich et al.,

2013).

Mathematical modeling of the cardiovascular

system using the ﬁnite element (FE) approach is an

useful too to estimate the cardiac mechanics and

wall stress, likely inhibiting CDM and PE. A few FE

modeling studies of the LV have validated stress

calculations by showing good agreement with

myocardial strain measured with implanted markers

(McCulloch et al., 1992); (Omens et al., 1993);

(Vetter and McCulloch, 2000). Guccione et al. have

639

Scardulla F., Rinaudo A., Scardulla C. and Pasta S..

Impact of Pericardial Effusion on Cardiac Mechanics in Patients with Dilated Cardiomyopathy.

DOI: 10.5220/0004615906390644

In Proceedings of the 3rd International Conference on Simulation and Modeling Methodologies, Technologies and Applications (BIOMED-2013), pages

639-644

ISBN: 978-989-8565-69-3

 2013 SCITEPRESS (Science and Technology Publications, Lda.)

successfully modeled end-isovolumic systole in an

ovine model of myocardial infarction and

determined material parameters that reproduced

circumferential stretching (as measured with 2D

tagged MRI) in the infarcted border zone (Guccione

et al., 2001).

The key role of wall stress in the progression of

LV remodeling was studied in DCM (Quarterman et

al., 2002); (Ratcliffe et al., 1998); (Zhong et al.,

2009). An increase in wall stress is known to reduce

myocardial fiber shortening, and increases in LV

wall stress have been reported in DCM. LV wall

stress is in part determined by the local curvature of

the ventricular wall (i.e., decreased curvature will

increase wall stress). In addition to increasing LV

size, CDM can alter myocardial properties and

normal LV shape curvature. The border zone will

have a higher stress, which makes it more

susceptible to ischemia and infarction and may

accelerate the remodeling process.

Therefore, the purpose of present study was to

assess the key role of wall stress and global function

of patients with CDM, PE. Cardiac mechanics was

thus compared to that of healthy patients with

normal wall thickness. We also tested the hypothesis

that pump function and wall stress in CDM can be

positively affected by the presence of a PE liquid.

2 MATERIALS AND METHODS

2.1 Imaging Procedure

We retrospectively identified patients with CDM

and PE who underwent magnetic resonance imaging

(MRI) from radiologic records of Mediterranean

Institute for Transplantation and Advanced

Specialized Therapies (ISMETT) and Ospedale

Riuniti Trieste. Patients underwent MRI as part of

their care, and not for the purpose of our study.

A series of long- and short-axis images of the

heart were obtained performing MR imaging

synchronized to the R wave of the electrocardiogram

signal. Short -axis slices were taken sequentially

every 6 mm until complete scanning of heart

chambers.

2.2 Heart Reconstruction

Endocardial and epicardial MRI surfaces of LV and

RV were segmented by contour lines using the

vascular modeling toolkit VMTK

(http://www.vmtk.org). Specifically, LV and RV

geometries were reconstructed at end-diastole (ED)

and end-systole (ES), which are defined as the

images with the maximum and minimum cross-

sectional area, respectively. Patients with PE

required also segmentation of the outer pericardial

layer. After segmentation process, endocardial and

epicardial surfaces of LV and RV were obtained by

loft protrusion of segmented contour lines.

2.3 FE Model

The space between the endocardial and epicardial

surfaces was meshed with 8-node brick elements to

generate a volumetric mesh in ABAQUS FE code.

Cardiac myoﬁber angles at the epicardium and

endocardium were assigned to be -60 degrees and 60

degrees, respectively (counterclockwise positive

when viewed from the epicardium).

Nearly incompressible, transversely isotropic,

hyperelastic constitutive laws for passive and active

myocardium was implemented in ABAQUS/Explicit

using a VUMAT subroutine (Ratcliffe et al., 1998).

Myocardial material parameters were estimated

comparing MRI measured and computationally

derived LV and RV volumes at ED and ES,

respectively. Manual iteration was used rather than

formal optimization. Similarly, PE was modeled as

isotropic, hyperelastic material which mechanical

properties were empirically found to match ED and

ES volumes of PE.

The basal node of LV were constrained along

long axis direction. The endocardial wall was loaded

at ED and ES pressure occurring at LV and RV. For

LV, ED pressure (P

) was 100 mmHg while ES

pressure (P

) was 25 mmHg. For RV, P

was 15

mmHg while P

was 30 mmHg.

2.4 Pressure-volume Relationships

and Stroke Volume

Chamber ED and ES volume (V

and V

)

solutions were used with the corresponding P

and

to plot the ED and ES pressure-volume

relationships (ESPVR and EDPVR, respectively),

which were then fit to appropriate polynomial

equations. The following linear equation was used to

estimate the ESPVR:



E







V





(1)

where E

is the end-systolic elastance and V

is the

volume intercept of the ESPVR, each determined by

linear regression of the data.

The polynomial equation used to estimate the

EDPVR was as follows:



E

,

E

,



E

,





(2)

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Applications

640

Figure 1: Representative map of average wall stress for (A) healthy patient, (B) CDM and (C) PE (solid grey indicates

liquid volume); models are not at same scale.

where E

0,ED

, E

1,ED

and E

2,ED

represent stiffness of the

LV diastolic compliance, again determined by linear

regression.

To determine global changes to pump function,

the stroke volume (SV)/P

and SV/V

relationships were calculated and plotted, assuming

that arterial elastance (E

) was constant. SV was

calculated according to the following equation:

 









1  



/



(3)

2.5 ED and ES Fiber Stress

For each simulation, stress in the local muscle fiber

direction was computed throughout the LV and RV

walls at end-diastole and end-systole of the pressure-

volume load. Thus, we evaluated the

average fiber stress has the mean value between the

longitudinal ﬁber stress and the cross-fiber stress.

3 RESULTS

Figure 1 shows representative distribution of

average fiber stress for patients with PE and CDM as

compared to the healthy patient. It can be observed

that ES LV stress is higher than that of RV, and this

occurs in the lateral side of LV chamber.

Differently, the patient with PE show higher ES wall

stress at the endocardial surface a cause of the liquid

constraining LV wall motion.

Maximum values of ES average fiber stress was

found markedly higher for patients with CDM

(105.5 kPa, n=3) compared to that of healthy patient

(20.9 kPa, n=2) and PE patient (42.9 kPa, n=2) as

shown by Figure 2. For both healthy and CDM

cases, maximum value of ED average fiber stress

was found drastically lower that those exhibited at

end-systolic phase (i.e., 13.5 kPa for healthy and

12.2 kPa for CDM). In contrast, ES fiber stress of

PE cases decreased up to 19.1 kPa.

For LV, CDM caused a leftward shift of both

EDVPR and ESPVR whereas PE induced a

rightward shift of these relationships as shown by

Fig. 3. Similar results are shown by RV. Starling

curve for CDM lies on the left compared to that of

both PE and healthy patients. Indeed, stroke volume

(Starling law) was reduced in CDM because the

decrease in diastolic compliance was not sufficiently

ImpactofPericardialEffusiononCardiacMechanicsinPatientswithDilatedCardiomyopathy

641

Figure 2: Comparison of maximum average wall stress

among patients with CDM and PE. Control, healthy

patient is also shown. Data are mean±SEM.

compensated by the improvements in end-systolic

elastance.

4 DISCUSSION

The present research demonstrates clearly that CDM

and PE alter differently both wall stress and cardiac

function when compared to healthy subject. Indeed,

the most striking finding is that the patient with PE

exhibits lower myocardial fiber stress and better

global function than those of the patient with CDM.

Therefore, both CMD and PE have important

implications in the mechanical changes of both LV

and RV chambers.

There are few studies on the wall stress and

cardiac function in CDM. Among these, Zhog et al.

investigated LV remodeling in ischemic CDM using

FE modeling (Zhong et al., 2009). They suggested

that LV remodeling in ischemic CDM is a multistep

process, which determines loss of contractile

function followed by acute dilatation of the

infarction area, increase of LV volume, lengthening

of the LV perimeter, and blunting of the normal

curvature. Wall stress were found increased in each

region of LV wall and has been shown to be a

measure of the afterload following infarction. These

findings are in agree with our distribution of wall

stress in CDM. Nevertheless, we found that ES wall

stress are 72% higher than that of healthy and PE

subjects, suggesting adverse clinical outcome for

this cardiac disease.

FE modeling has been widely used to study

cardiac diseases, and this has led to an improved

integrative understanding of the heart system. For

instance, Wenk et al. evinced that residual stress

produced by ventricular volume reduction surgery

has a little effect on the LV function and cardiac

mechanics (Wenk et al., 2010). Another study

suggests that surgical anterior ventricular restoration

reduces myoﬁber stress in the akinetic infarct at the

expense of a reduction in the Starling relationship

(Jhun et al., 2010). FE analysis also demonstrated

that aneurysm implication decreases ﬁber stress

without depressing stroke volume (Guccione et al.,

2001); (Walker et al., 2005). Recently, Carrick et al.

highlighted that Coapsys procedure decreases

myoﬁber stress at ED and ES, and that the

improvement in myoﬁber stress may contribute to

the long-term effect of Coapsys on LV remodeling

(Carrick et al., 2012).

In tissue engineering approach, FE simulation

indicated that the addition of non-contractile

material to a damaged LV wall has important effects

on cardiac mechanics, with potentially beneficial

reduction of elevated myofiber stresses, as well as

confounding changes to clinical left ventricular

metrics (Wall et al., 2006). This study therefore

supports our hypothesis that that pump function and

wall stress in CDM may be improved by

surrounding the epicardial layer with liquid as it

occurs in PE. This is also confirmed by clinical

evidence in patients with liquid accumulation for

which the global pressure-volume relationships is

shift further to the left as suggested by our

computational model.

6 MODEL LIMITATIONS

Although this model captures many aspects of LV

and RV mechanics in both CDM and PE, limitations

still exist. One significant limitation is that wall

thickness between patients with CDM and PE were

different.

This likely influences the wall stress which is

given by the ratio of the pressure exerted on the LV

endocardio on wall thickness. Indeed, patient with

PE had a LV wall thickness of 8.5 mm which is

higher than that of CDM (i.e., 5.7 mm). Future study

needs patient comparison at matched values of LV

wall thickness.

Other limits include calculation of regional

myocardial material properties as well as restricted

number of patients. In spite of this limitations, these

findings provide relevant insight on the cardiac

mechanics of patients with CDM and PE.

Healthy CDM PE

Max Average Fiber Stress (kPa)

200

250

300

(n=3)

(n=2) (n=2)

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Figure 3: Representative cardiac function for a patient of each group: (A) LV pressure-volume relationships, (B) RV

pressure-volume relationships, (C) LV stroke volume on ED pressure and (D) LV stroke volume on ED volume.

7 CONCLUSIONS

This study suggests that CDM and PE conversely

alter both wall stress distribution and global cardiac

function. The reduction in the myoﬁber stress caused

by liquid accumulation on the pericardial layer may

contribute to the long-term clinical outcome of

patient with PE.

ACKNOWLEDGEMENTS

The authors thank Mr. Armando Pasta of ISMETT

for his technical assistance with image acquisition.

This study was funded in part by a grant from

Fondazione RiMED provided to Dr. Pasta.

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