Trabeculae carneae are irregular structures that cover the endocardial surfaces of both ventricles and account for a significant portion of human ventricular mass. The role of trabeculae carneae in diastolic and systolic functions of the left ventricle (LV) is not well understood. Thus, the objective of this study was to investigate the functional role of trabeculae carneae in the LV. Finite element (FE) analyses of ventricular functions were conducted for three different models of human LV derived from high-resolution magnetic resonance imaging (MRI). The first model comprised trabeculae carneae and papillary muscles, while the second model had papillary muscles and partial trabeculae carneae, and the third model had a smooth endocardial surface. We customized these patient-specific models with myofiber architecture generated with a rule-based algorithm, diastolic material parameters of Fung strain energy function derived from biaxial tests and adjusted with the empirical Klotz relationship, and myocardial contractility constants optimized for average normal ejection fraction (EF) of the human LV. Results showed that the partial trabeculae cutting model had enlarged end-diastolic volume (EDV), reduced wall stiffness, and even increased end-systolic function, indicating that the absence of trabeculae carneae increased the compliance of the LV during diastole, while maintaining systolic function.

References

1.
Goo
,
S.
,
Joshi
,
P.
,
Sands
,
G.
,
Gerneke
,
D.
,
Taberner
,
A.
,
Dollie
,
Q.
,
LeGrice
,
I.
, and
Loiselle
,
D.
,
2009
, “
Trabeculae Carneae as Models of the Ventricular Walls: Implications for the Delivery of Oxygen
,”
J. Gen. Physiol.
,
134
(
4
), pp.
339
350
.
2.
Janik
,
M.
,
Cham
,
M. D.
,
Ross
,
M. I.
,
Wang
,
Y.
,
Codella
,
N.
,
Min
,
J. K.
,
Prince
,
M. R.
,
Manoushagian
,
S.
,
Okin
,
P. M.
,
Devereux
,
R. B.
, and
Weinsaft
,
J. W.
,
2008
, “
Effects of Papillary Muscles and Trabeculae on Left Ventricular Quantification: Increased Impact of Methodological Variability in Patients With Left Ventricular Hypertrophy
,”
J. Hypertens.
,
26
(
8
), pp.
1677
1685
.
3.
Serrani
,
M.
,
Costantino
,
M. L.
, and
Fumero
,
R.
,
2013
, “
The Influence of Cardiac Trabeculae on Ventricular Mechanics
,”
Comput. Cardiol.
,
40
, pp.
811
814
.https://ieeexplore.ieee.org/document/6713501
4.
Sedmera
,
D.
,
Pexieder
,
T.
,
Vuillemin
,
M.
,
Thompson
,
R. P.
, and
Anderson
,
R. H.
,
2000
, “
Developmental Patterning of the Myocardium
,”
Anat. Rec.
,
258
(
4
), pp.
319
337
.
5.
Wenink
,
A. C.
, and
Gittenberger-de Groot
,
A. C.
,
1982
, “
Left and Right Ventricular Trabecular Patterns: Consequence of Ventricular Septation and Valve Development
,”
Br. Heart J.
,
48
(
5
), pp.
462
468
.
6.
Bartram
,
U.
,
Bauer
,
J.
, and
Schranz
,
D.
,
2007
, “
Primary Noncompaction of the Ventricular Myocardium From the Morphogenetic Standpoint
,”
Pediatr. Cardiol.
,
28
(
5
), pp.
325
332
.
7.
Captur
,
G.
,
Wilson
,
R.
,
Bennett
,
M. F.
,
Luxan
,
G.
,
Nasis
,
A.
,
de la Pompa
,
J. L.
,
Moon
,
J. C.
, and
Mohun
,
T. J.
,
2016
, “
Morphogenesis of Myocardial Trabeculae in the Mouse Embryo
,”
J. Anat.
,
229
(
2
), pp.
314
325
.
8.
Halaney
,
D. L.
,
Sanyal
,
A.
,
Nafissi
,
N. A.
,
Escobedo
,
D.
,
Goros
,
M.
,
Michalek
,
J.
,
Acevedo
,
P. J.
,
Pérez
,
W.
,
Patricia Escobar
,
G.
,
Feldman
,
M. D.
, and
Han
,
H.-C.
,
2017
, “
The Effect of Trabeculae Carneae on Left Ventricular Diastolic Compliance: Improvement in Compliance With Trabecular Cutting
,”
ASME J. Biomech. Eng.
,
139
(
3
), p.
031012
.
9.
Lin
,
L. Y.
,
Su
,
M. Y.
,
Pham
,
V. T.
,
Tran
,
T. T.
,
Wang
,
Y. H.
,
Tseng
,
W. Y.
,
Lo
,
M. T.
, and
Lin
,
J. L.
,
2016
, “
Endocardial Remodeling in Heart Failure Patients With Impaired and Preserved Left Ventricular Systolic Function—A Magnetic Resonance Image Study
,”
Sci. Rep.
,
6
, p.
20868
.
10.
Jacquier
,
A.
,
Thuny
,
F.
,
Jop
,
B.
,
Giorgi
,
R.
,
Cohen
,
F.
,
Gaubert
,
J. Y.
,
Vidal
,
V.
,
Bartoli
,
J. M.
,
Habib
,
G.
, and
Moulin
,
G.
,
2010
, “
Measurement of Trabeculated Left Ventricular Mass Using Cardiac Magnetic Resonance Imaging in the Diagnosis of Left Ventricular Non-Compaction
,”
Eur. Heart J.
,
31
(
9
), pp.
1098
1104
.
11.
Moore
,
B.
, and
Prasad Dasi
,
L.
,
2013
, “
Quantifying Left Ventricular Trabeculae Function–Application of Image‐Based Fractal Analysis
,”
Physiol. Rep.
,
1
(
4
), p. e00068.
12.
Spreeuwers
,
L. J.
,
Bangma
,
S. J.
,
Meerwaldt
,
R. J. H. W.
,
Vonken
,
E. J.
, and
Breeuwer
,
M.
,
2005
, “
Detection of Trabeculae and Papillary Muscles in Cardiac MR Images
,”
Computers in Cardiology
, Lyon, France, Sept. 25–28, pp.
415
418
.
13.
Vedula
,
V.
,
Seo
,
J.-H.
,
Lardo
,
A. C.
, and
Mittal
,
R.
,
2016
, “
Effect of Trabeculae and Papillary Muscles on the Hemodynamics of the Left Ventricle
,”
Theor. Comput. Fluid Dyn.
,
30
(
1–2
), pp.
3
21
.
14.
Bishop
,
M. J.
,
Plank
,
G.
,
Burton
,
R. A.
,
Schneider
,
J. E.
,
Gavaghan
,
D. J.
,
Grau
,
V.
, and
Kohl
,
P.
,
2010
, “
Development of an Anatomically Detailed MRI-Derived Rabbit Ventricular Model and Assessment of Its Impact on Simulations of Electrophysiological Function
,”
Am. J. Physiol. Heart Circ. Physiol.
,
298
(
2
), pp.
H699
H718
.
15.
Clarke
,
G. D.
,
Solis-Herrera
,
C.
,
Molina-Wilkins
,
M.
,
Martinez
,
S.
,
Merovci
,
A.
,
Cersosimo
,
E.
,
Chilton
,
R. J.
,
Iozzo
,
P.
,
Gastaldelli
,
A.
,
Abdul-Ghani
,
M.
, and
DeFronzo
,
R. A.
,
2017
, “
Pioglitazone Improves Left Ventricular Diastolic Function in Subjects With Diabetes
,”
Diabetes Care
,
40
(
11
), pp.
1530
1536
.
16.
Guccione
,
J. M.
,
Costa
,
K. D.
, and
McCulloch
,
A. D.
,
1995
, “
Finite Element Stress Analysis of Left Ventricular Mechanics in the Beating Dog Heart
,”
J. Biomech.
,
28
(
10
), pp.
1167
1177
.
17.
Voorhees
,
A. P.
, and
Han
,
H. C.
,
2014
, “
A Model to Determine the Effect of Collagen Fiber Alignment on Heart Function Post Myocardial Infarction
,”
Theor. Biol. Med. Model.
,
11
, p.
6
.
18.
Fatemifar
,
F.
,
Feldman
,
M.
, and
Han
,
H.-C.
,
2017
, “
Characterization of Biomechanical Properties of Human Trabeculae Carneae
,”
Summer Biomechanics, Bioengineering and Biotransport Conference (SB3C 2017)
, Tucson, AZ, June 21–24.
19.
Fatemifar
,
F.
,
Feldman
,
M.
,
Oglesby
,
M.
, and
Han
,
H. C.
,
2018
, “
Comparison of Biomechanical Properties and Microstructure of Trabeculae Carneae, Papillary Muscles, and Myocardium in Human Heart
,”
ASME J. Biomech. Eng.
,
141
(
2
), p.
021007
.
20.
Klotz
,
S.
,
Dickstein
,
M. L.
, and
Burkhoff
,
D.
,
2007
, “
A Computational Method of Prediction of the End-Diastolic Pressure-Volume Relationship by Single Beat
,”
Nat. Protoc.
,
2
(
9
), pp.
2152
2158
.
21.
Klotz
,
S.
,
Hay
,
I.
,
Dickstein
,
M. L.
,
Yi
,
G. H.
,
Wang
,
J.
,
Maurer
,
M. S.
,
Kass
,
D. A.
, and
Burkhoff
,
D.
,
2006
, “
Single-Beat Estimation of End-Diastolic Pressure-Volume Relationship: A Novel Method With Potential for Noninvasive Application
,”
Am. J. Physiol. Heart Circ. Physiol.
,
291
(
1
), pp.
H403
H412
.
22.
Guccione
,
J. M.
, and
McCulloch
,
A. D.
,
1993
, “
Mechanics of Active Contraction in Cardiac Muscle—Part I: Constitutive Relations for Fiber Stress That Describe Deactivation
,”
ASME J. Biomech. Eng.
,
115
(
1
), pp.
72
81
.https://biomechanical.asmedigitalcollection.asme.org/article.aspx?articleid=1399040
23.
Guccione
,
J. M.
,
Waldman
,
L. K.
, and
McCulloch
,
A. D.
,
1993
, “
Mechanics of Active Contraction in Cardiac Muscle—Part II: Cylindrical Models of the Systolic Left Ventricle
,”
ASME J. Biomech. Eng.
,
115
(
1
), pp.
82
90
.
24.
Maas
,
S. A.
,
Ellis
,
B. J.
,
Ateshian
,
G. A.
, and
Weiss
,
J. A.
,
2012
, “
FEBio: Finite Elements for Biomechanics
,”
ASME J. Biomech. Eng.
,
134
(
1
), p.
011005
.
25.
Maceira
,
A. M.
,
Prasad
,
S. K.
,
Khan
,
M.
, and
Pennell
,
D. J.
,
2006
, “
Normalized Left Ventricular Systolic and Diastolic Function by Steady State Free Precession Cardiovascular Magnetic Resonance
,”
J. Cardiovasc. Magn. Reson. Off. J. Soc. Cardiovasc. Magn. Reson.
,
8
(
3
), pp.
417
426
.
26.
Kawel-Boehm
,
N.
,
Maceira
,
A.
,
Valsangiacomo-Buechel
,
E. R.
,
Vogel-Claussen
,
J.
,
Turkbey
,
E. B.
,
Williams
,
R.
,
Plein
,
S.
,
Tee
,
M.
,
Eng
,
J.
, and
Bluemke
,
D. A.
,
2015
, “
Normal Values for Cardiovascular Magnetic Resonance in Adults and Children
,”
J. Cardiovasc. Magn. Reson.
,
17
(
1
), p.
29
.
27.
Lee
,
L. C.
,
Wenk
,
J. F.
,
Zhong
,
L.
,
Klepach
,
D.
,
Zhang
,
Z.
,
Ge
,
L.
,
Ratcliffe
,
M. B.
,
Zohdi
,
T. I.
,
Hsu
,
E.
,
Navia
,
J. L.
,
Kassab
,
G. S.
, and
Guccione
,
J. M.
,
2013
, “
Analysis of Patient-Specific Surgical Ventricular Restoration: Importance of an Ellipsoidal Left Ventricular Geometry for Diastolic and Systolic Function
,”
J. Appl. Physiol.
,
115
(
1
), pp.
136
144
.
28.
Potse
,
M.
,
Dube
,
B.
,
Richer
,
J.
,
Vinet
,
A.
, and
Gulrajani
,
R. M.
,
2006
, “
A Comparison of Monodomain and Bidomain Reaction-Diffusion Models for Action Potential Propagation in the Human Heart
,”
IEEE Trans. Bio-Med. Eng.
,
53
(
12
), pp.
2425
2435
.
29.
Carapella
,
V.
,
Bordas
,
R.
,
Pathmanathan
,
P.
,
Schneider
,
J. E.
,
Kohl
,
P.
,
Burrage
,
K.
, and
Grau
,
V.
,
2013
, “
Effect of Fibre Orientation Optimisation in an Electromechanical Model of Left Ventricular Contraction in Rat
,”
Functional Imaging and Modeling of the Heart: Seventh International Conference
(FIMH), London, UK, June 20–22, pp.
46
53
.
30.
Wang
,
H. M.
,
Gao
,
H.
,
Luo
,
X. Y.
,
Berry
,
C.
,
Griffith
,
B. E.
,
Ogden
,
R. W.
, and
Wang
,
T. J.
,
2013
, “
Structure-Based Finite Strain Modelling of the Human Left Ventricle in Diastole
,”
Int. J. Numer. Methods Biomed. Eng.
,
29
(
1
), pp.
83
103
.
31.
Bishop
,
M. J.
,
Hales
,
P.
,
Plank
,
G.
,
Gavaghan
,
D. J.
,
Scheider
,
J.
, and
Grau
,
V.
,
2009
, “
Comparison of Rule-Based and DTMRI-Derived Fibre Architecture in a Whole Rat Ventricular Computational Model
,” Functional Imaging and Modeling of the Heart, N. Ayache, H. Delingette, and M. Sermesant, eds., Springer, Berlin, pp. 87–96.
32.
Mekkaoui
,
C.
,
Huang
,
S.
,
Chen
,
H. H.
,
Dai
,
G.
,
Reese
,
T. G.
,
Kostis
,
W. J.
,
Thiagalingam
,
A.
,
Maurovich-Horvat
,
P.
,
Ruskin
,
J. N.
,
Hoffmann
,
U.
,
Jackowski
,
M. P.
, and
Sosnovik
,
D. E.
,
2012
, “
Fiber Architecture in Remodeled Myocardium Revealed With a Quantitative Diffusion CMR Tractography Framework and Histological Validation
,”
J. Cardiovasc. Magn. Reson.
,
14
(
1
), p.
70
.
33.
Kim
,
H. J.
,
Yoon
,
J. H.
,
Lee
,
E. J.
,
Oh
,
J. H.
,
Lee
,
J. Y.
,
Lee
,
S. J.
, and
Han
,
J. W.
,
2015
, “
Normal Left Ventricular Torsion Mechanics in Healthy Children: Age Related Changes of Torsion Parameters Are Closely Related to Changes in Heart Rate
,”
Korean Circ. J.
,
45
(
2
), pp.
131
140
.
34.
ten Brinke
,
E. A.
,
Klautz
,
R. J.
,
Verwey
,
H. F.
,
van der Wall
,
E. E.
,
Dion
,
R. A.
, and
Steendijk
,
P.
,
2010
, “
Single-Beat Estimation of the Left Ventricular End-Systolic Pressure-Volume Relationship in Patients With Heart Failure
,”
Acta Physiol. (Oxford, Engl.)
,
198
(
1
), pp.
37
46
.
35.
Dorri
,
F.
,
Niederer
,
P. F.
, and
Lunkenheimer
,
P. P.
,
2006
, “
A Finite Element Model of the Human Left Ventricular Systole
,”
Comput. Methods Biomech. Biomed. Eng.
,
9
(
5
), pp.
319
341
.
36.
Chengode
,
S.
,
2016
, “
Left Ventricular Global Systolic Function Assessment by Echocardiography
,”
Ann. Card. Anaesth.
,
19
(
5
), pp.
26
S34
.
37.
Moore
,
C. C.
,
Lugo-Olivieri
,
C. H.
,
McVeigh
,
E. R.
, and
Zerhouni
,
E. A.
,
2000
, “
Three-Dimensional Systolic Strain Patterns in the Normal Human Left Ventricle: Characterization With Tagged MR Imaging
,”
Radiology
,
214
(
2
), pp.
453
466
.
38.
Krishnamurthy
,
A.
,
Villongco
,
C. T.
,
Chuang
,
J.
,
Frank
,
L. R.
,
Nigam
,
V.
,
Belezzuoli
,
E.
,
Stark
,
P.
,
Krummen
,
D. E.
,
Narayan
,
S.
,
Omens
,
J. H.
,
McCulloch
,
A. D.
, and
Kerckhoffs
,
R. C.
,
2013
, “
Patient-Specific Models of Cardiac Biomechanics
,”
J. Comput. Phys.
,
244
, pp.
4
21
.
39.
Genet
,
M.
,
Lee
,
L. C.
,
Nguyen
,
R.
,
Haraldsson
,
H.
,
Acevedo-Bolton
,
G.
,
Zhang
,
Z.
,
Ge
,
L.
,
Ordovas
,
K.
,
Kozerke
,
S.
, and
Guccione
,
J. M.
,
2014
, “
Distribution of Normal Human Left Ventricular Myofiber Stress at End Diastole and End Systole: A Target for in Silico Design of Heart Failure Treatments
,”
J. Appl. Physiol.
,
117
(
2
), pp.
142
152
.
40.
Dang
,
A. B.
,
Guccione
,
J. M.
,
Zhang
,
P.
,
Wallace
,
A. W.
,
Gorman
,
R. C.
,
Gorman
,
J. H.
, III
, and
Ratcliffe
,
M. B.
,
2005
, “
Effect of Ventricular Size and Patch Stiffness in Surgical Anterior Ventricular Restoration: A Finite Element Model Study
,”
Ann. Thorac. Surg.
,
79
(
1
), pp.
185
193
.
41.
Oglesby
,
M.
,
Escobedo
,
D.
,
Escobar
,
G. P.
,
Fatemifar
,
F.
,
Bailey
,
S. R.
,
Han
,
H. C.
, and
Feldman
,
M. D.
,
2019
, “
Trabecular Cutting: A Novel Surgical Therapy to Increase Diastolic Compliance
,”
J. Appl. Physiol.
(in press).
42.
Strauer
,
B. E.
,
Beer
,
K.
,
Heitlinger
,
K.
, and
Hofling
,
B.
,
1977
, “
Left Ventricular Systolic Wall Stress as a Primary Determinant of Myocardial Oxygen Consumption: Comparative Studies in Patients With Normal Left Ventricular Function, With Pressure and Volume Overload and With Coronary Heart Disease
,”
Basic Res. Cardiol.
,
72
(
2–3
), pp.
306
313
.
43.
Shen
,
M. Y.
,
Liu
,
Y. H.
,
Sinusas
,
A. J.
,
Fetterman
,
R.
,
Bruni
,
W.
,
Drozhinin
,
O. E.
,
Zaret
,
B. L.
, and
Wackers
,
F. J.
,
1999
, “
Quantification of Regional Myocardial Wall Thickening on Electrocardiogram-Gated SPECT Imaging
,”
J. Nucl. Cardiol.: Off. Publ. Am. Soc. Nucl. Cardiol.
,
6
(
6
), pp.
583
595
.
44.
Omar
,
A. M.
,
Vallabhajosyula
,
S.
, and
Sengupta
,
P. P.
,
2015
, “
Left Ventricular Twist and Torsion: Research Observations and Clinical Applications
,”
Circ. Cardiovasc. Imaging
,
8
(
6
), pp. 74–82.
45.
Nucifora
,
G.
,
Muser
,
D.
,
Morocutti
,
G.
,
Piccoli
,
G.
,
Zanuttini
,
D.
,
Gianfagna
,
P.
, and
Proclemer
,
A.
,
2014
, “
Disease-Specific Differences of Left Ventricular Rotational Mechanics Between Cardiac Amyloidosis and Hypertrophic Cardiomyopathy
,”
Am. J. Physiol.-Heart Circ. Physiol.
,
307
(
5
), pp.
H680
H688
.
46.
Sengupta
,
P. P.
,
Khandheria
,
B. K.
, and
Narula
,
J.
,
2008
, “
Twist and Untwist Mechanics of the Left Ventricle
,”
Heart Failure Clin.
,
4
(
3
), pp.
315
324
.
47.
Saito
,
M.
,
Okayama
,
H.
,
Yoshii
,
T.
,
Hiasa
,
G.
,
Sumimoto
,
T.
,
Inaba
,
S.
,
Nishimura
,
K.
,
Inoue
,
K.
,
Ogimoto
,
A.
,
Ohtsuka
,
T.
,
Funada
,
J.
,
Shigematsu
,
Y.
, and
Higaki
,
J.
,
2011
, “
The Differences in Left Ventricular Torsional Behavior Between Patients With Hypertrophic Cardiomyopathy and Hypertensive Heart Disease
,”
Int. J. Cardiol.
,
150
(
3
), pp.
301
306
.
48.
Nakatani
,
S.
,
2011
, “
Left Ventricular Rotation and Twist: Why Should We Learn?
,”
J. Cardiovasc. Ultrasound
,
19
(
1
), pp.
1
6
.
49.
Wang
,
J.
,
Khoury
,
D. S.
,
Yue
,
Y.
,
Torre-Amione
,
G.
, and
Nagueh
,
S. F.
,
2007
, “
Left Ventricular Untwisting Rate by Speckle Tracking Echocardiography
,”
Circulation
,
116
(
22
), pp.
2580
2586
.
50.
Heinzel
,
F. R.
,
Hohendanner
,
F.
,
Jin
,
G.
,
Sedej
,
S.
, and
Edelmann
,
F.
,
2015
, “
Myocardial Hypertrophy and Its Role in Heart Failure With Preserved Ejection Fraction
,”
J. Appl. Physiol.
,
119
(
10
), pp.
1233
1242
.
51.
LeWinter
,
M. M.
, and
Meyer
,
M.
,
2013
, “
Mechanisms of Diastolic Dysfunction in HFpEF: If It's Not One Thing It's Another
,”
Circ. Heart Failure
,
6
(
6
), pp.
1112
1115
.
52.
Eberli
,
F. R.
,
Strömer
,
H.
,
Ferrell
,
M. A.
,
Varma
,
N.
,
Morgan
,
J. P.
,
Neubauer
,
S.
, and
Apstein
,
C. S.
,
2000
, “
Lack of Direct Role for Calcium in Ischemic Diastolic Dysfunction in Isolated Hearts
,”
Circulation
,
102
(
21
), pp.
2643
2649
.
53.
Varma
,
N.
,
Eberli
,
F. R.
, and
Apstein
,
C. S.
,
2001
, “
Left Ventricular Diastolic Dysfunction During Demand Ischemia: Rigor Underlies Increased Stiffness Without Calcium-Mediated Tension. Amelioration by Glycolytic Substrate
,”
J. Am. Coll. Cardiol.
,
37
(
8
), pp.
2144
2153
.
54.
Franz
,
I. W.
,
Tonnesmann
,
U.
, and
Muller
,
J. F.
,
1998
, “
Time Course of Complete Normalization of Left Ventricular Hypertrophy During Long-Term Antihypertensive Therapy With Angiotensin Converting Enzyme Inhibitors
,”
Am. J. Hypertens.
,
11
(
6
), pp.
631
639
.
55.
Fernandez-Golfin
,
C.
,
Pachon
,
M.
,
Corros
,
C.
,
Bustos
,
A.
,
Cabeza
,
B.
,
Ferreiros
,
J.
,
de Isla
,
L. P.
,
Macaya
,
C.
, and
Zamorano
,
J.
,
2009
, “
Left Ventricular Trabeculae: Quantification in Different Cardiac Diseases and Impact on Left Ventricular Morphological and Functional Parameters Assessed With Cardiac Magnetic Resonance
,”
J. Cardiovasc. Med.
,
10
(
11
), pp.
827
833
.
56.
Han
,
H. C.
,
Oshinski
,
J. N.
,
Ku
,
D. N.
, and
Pettigrew
,
R. I.
,
2002
, “
A Left Ventricle Model to Predict Post-Revascularization Ejection Fraction Based on Cine Magnetic Resonance Images
,”
ASME J. Biomech. Eng.
,
124
(
1
), pp.
52
55
.
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