Abstract

Pressure overload (PO) and volume overload (VO) of the heart result in distinctive changes to geometry, due to compensatory structural remodeling. This remodeling potentially leads to changes in tissue mechanical properties. Understanding such changes is important, as tissue modulus has an impact on cardiac performance, disease progression, and influences on cell phenotype. Pressure–volume (PV) loop analysis, a clinically relevant method for measuring left ventricular (LV) chamber stiffness, was performed in vivo on control rat hearts and rats subjected to either chronic PO through Angiotensin-II infusion (4-weeks) or VO (8-weeks). Immediately following PV loops, biaxial testing was performed on LV free wall tissue to directly measure tissue mechanical properties. The β coefficient, an index of chamber stiffness calculated from the PV loop analysis, increased 98% in PO (n = 4) and decreased 38% in VO (n = 5) compared to control (n = 6). Material constants of LV walls obtained from ex vivo biaxial testing (n = 9–10) were not changed in Angiotensin-II induced PO and decreased by about half in VO compared to control (47% in the circumferential and 57% the longitudinal direction). PV loop analysis showed the expected increase in chamber stiffness of PO and expected decrease in chamber stiffness of VO. Biaxial testing showed a decreased modulus of the myocardium of the VO model, but no changes in the PO model, this suggests the increased chamber stiffness in PO, as shown in the PV loop analysis, may be secondary to changes in tissue mass and/or geometry but not an increase in passive tissue mechanical properties.

References

1.
Thiedemann
,
K.-U.
,
Holubarsch
,
C.
,
Medugorac
,
I.
, and
Jacob
,
R.
,
1983
, “
Cardiology Connective Tissue Content and Myocardial Stiffness in Pressure Overload Hypertrophy a Combined Study of Morphologic, Morphometric, Biochemical, and Mechanical Parameters
,”
Basic Res. Cardiol.
,
78
(
2
), pp.
140
155
.10.1007/BF01906668
2.
Chaturvedi
,
R. R.
,
Herron
,
T.
,
Simmons
,
R.
,
Shore
,
D.
,
Kumar
,
P.
,
Sethia
,
B.
,
Chua
,
F.
,
Vassiliadis
,
E.
, and
Kentish
,
J. C.
,
2010
, “
Passive Stiffness of Myocardium From Congenital Heart Disease and Implications for Diastole
,”
Circulation
,
121
(
8
), pp.
979
988
.10.1161/CIRCULATIONAHA.109.850677
3.
Hutchinson
,
K. R.
,
Guggilam
,
A.
,
Cismowski
,
M. J.
,
Galantowicz
,
M. L.
,
West
,
T. A.
,
Stewart
,
J. A.
,
Zhang
,
X.
,
Lord
,
K. C.
, and
Lucchesi
,
P. A.
,
2011
, “
Temporal Pattern of Left Ventricular Structural and Functional Remodeling Following Reversal of Volume Overload Heart Failure
,”
J. Appl. Physiol.
,
111
(
6
), pp.
1778
1788
.10.1152/japplphysiol.00691.2011
4.
Childers
,
R. C.
,
Sunyecz
,
I.
,
West
,
T. A.
,
Cismowski
,
M. J.
,
Lucchesi
,
P. A.
, and
Gooch
,
K. J.
,
2019
, “
Role of the Cytoskeleton in the Development of a Hypofibrotic Cardiac Fibroblast Phenotype in Volume Overload Heart Failure
,”
Am. J. Physiol. Circ. Physiol.
,
316
(
3
), pp.
H596
H608
.10.1152/ajpheart.00095.2018
5.
Forte
,
G.
,
Pagliari
,
S.
,
Ebara
,
M.
,
Uto
,
K.
,
Van Tam
,
J. K.
,
Romanazzo
,
S.
,
Escobedo-Lucea
,
C.
,
Romano
,
E.
,
Di Nardo
,
P.
,
Traversa
,
E.
, and
Aoyagi
,
T.
,
2012
, “
Substrate Stiffness Modulates Gene Expression and Phenotype in Neonatal Cardiomyocytes In Vitro
,”
Tissue Eng. Part A
,
18
(
17–18
), pp.
1837
1848
.10.1089/ten.tea.2011.0707
6.
Galie
,
P. A.
,
Khalid
,
N.
,
Carnahan
,
K. E.
,
Westfall
,
M. V.
, and
Stegemann
,
J. P.
,
2013
, “
Substrate Stiffness Affects Sarcomere and Costamere Structure and Electrophysiological Function of Isolated Adult Cardiomyocytes
,”
Cardiovasc. Pathol.
,
22
(
3
), pp.
219
227
.10.1016/j.carpath.2012.10.003
7.
Jacot
,
J. G.
,
McCulloch
,
A. D.
, and
Omens
,
J. H.
,
2008
, “
Substrate Stiffness Affects the Functional Maturation of Neonatal Rat Ventricular Myocytes
,”
Biophys. J.
,
95
(
7
), pp.
3479
3487
.10.1529/biophysj.107.124545
8.
Sarrazy
,
V.
,
Koehler
,
A.
,
Chow
,
M. L.
,
Zimina
,
E.
,
Li
,
C. X.
,
Kato
,
H.
,
Caldarone
,
C. A.
, and
Hinz
,
B.
,
2014
, “
Integrins Αvβ5 and Αvβ3 Promote Latent TGF-Β1 Activation by Human Cardiac Fibroblast Contraction
,”
Cardiovasc. Res.
,
102
(
3
), pp.
407
417
.10.1093/cvr/cvu053
9.
Xie
,
J.
,
Zhang
,
Q.
,
Zhu
,
T.
,
Zhang
,
Y.
,
Liu
,
B.
,
Xu
,
J.
, and
Zhao
,
H.
,
2014
, “
Substrate Stiffness-Regulated Matrix Metalloproteinase Output in Myocardial Cells and Cardiac Fibroblasts: Implications for Myocardial Fibrosis
,”
Acta Biomater.
,
10
(
6
), pp.
2463
2472
.10.1016/j.actbio.2014.01.031
10.
Hutchinson
,
K. R.
,
Saripalli
,
C.
,
Chung
,
C. S.
, and
Granzier
,
H.
,
2015
, “
Increased Myocardial Stiffness Due to Cardiac Titin Isoform Switching in a Mouse Model of Volume Overload Limits Eccentric Remodeling
,”
J. Mol. Cell. Cardiol.
,
79
, pp.
104
114
.10.1016/j.yjmcc.2014.10.020
11.
De Stefano
,
L. M.
,
Matsubara
,
L. S.
, and
Matsubara
,
B. B.
,
2006
, “
Myocardial Dysfunction With Increased Ventricular Compliance in Volume Overload Hypertrophy
,”
Eur. J. Heart Fail.
,
8
(
8
), pp.
784
789
.10.1016/j.ejheart.2006.02.005
12.
Norton
,
G. R.
,
Tsotetsi
,
J.
,
Trifunovic
,
B.
,
Hartford
,
C.
,
Candy
,
G. P.
, and
Woodiwiss
,
A. J.
,
1997
, “
Myocardial Stiffness is Attributed to Alterations in Cross-Linked Collagen Rather Than Total Collagen or Phenotypes in Spontaneously Hypertensive Rats
,”
Circulation
,
96
(
6
), pp.
1991
1998
.10.1161/01.CIR.96.6.1991
13.
Grossman
,
W.
,
Mclaurin
,
L. P.
, and
Stefadouros
,
M. A.
,
1974
, “
Left Ventricular Stiffness Associated With Chronic Pressure and Volume Overloads in Man
,”
Circ. Res.
,
35
(
5
), pp.
793
800
.10.1161/01.RES.35.5.793
14.
Esfandiari
,
S.
,
Fuchs
,
F.
,
Wainstein
,
R. V.
,
Chelvanathan
,
A.
,
Mitoff
,
P.
,
Sasson
,
Z.
, and
Mak
,
S.
,
2015
, “
Heart Rate-Dependent Left Ventricular Diastolic Function in Patients With and Without Heart Failure
,”
J. Card. Fail.
,
21
(
1
), pp.
68
75
.10.1016/j.cardfail.2014.10.013
15.
Hoskins
,
A. C.
,
Jacques
,
A.
,
Bardswell
,
S. C.
,
Mckenna
,
W. J.
,
Tsang
,
V.
,
Dos Remedios
,
C. G.
,
Ehler
,
E.
,
Adams
,
K.
,
Jalilzadeh
,
S.
,
Avkiran
,
M.
,
Watkins
,
H.
,
Redwood
,
C.
,
Marston
,
S. B.
, and
Kentish
,
J. C.
,
2010
, “
Normal Passive Viscoelasticity but Abnormal Myofibrillar Force Generation in Human Hypertrophic Cardiomyopathy
,”
J. Mol. Cell. Cardiol.
, 49(5), pp.
737
745
.10.1016/j.yjmcc.2010.06.006
16.
Kato
,
S.
,
Koide
,
M.
,
Cooper
,
G.
, and
Zile
,
M. R.
,
1996
, “
Effects of Pressure- or Volume-Overload Hypertrophy on Passive Stiffness in Isolated Adult Cardiac Muscle Cells
,”
Am. J. Physiol.: Hear. Circ. Physiol.
,
271
(
6
), pp.
2575
2582
.10.1152/ajpheart.1996.271.6.H2575
17.
Williams
,
J. F.
,
Mathew
,
B.
,
Hern
,
D. L.
,
Potter
,
R. D.
, and
Deiss
,
W. P.
,
1983
, “
Myocardial Hydroxyproline and Mechanical Response to Prolonged Pressure Loading Followed by Unloading in the Cat
,”
J. Clin. Invest.
,
72
(
6
), pp.
1910
1917
.10.1172/JCI111154
18.
Javani
,
S.
,
Gordon
,
M.
, and
Azadani
,
A. N.
,
2016
, “
Biomechanical Properties and Microstructure of Heart Chambers: A Paired Comparison Study in an Ovine Model
,”
Ann. Biomed. Eng.
, 44(11), pp.
3266
3283
.10.1007/s10439-016-1658-7
19.
Smaill
,
B.
, and
Hunter
,
P.
,
1991
,
Structure and Function of the Diastolic Heart: Material Properties of Passive Myocardium
,
Springer
,
New York
, pp.
1
29
.
20.
Sommer
,
G.
,
Haspinger
,
D. C.
,
Andra
,
M.
,
Sacherer
,
M.
,
Viertler
,
C.
,
Regitnig
,
P.
, and
Holzapfel
,
G. A.
,
2015
, “
Quantification of Shear Deformations and Corresponding Stresses in the Biaxially Tested Human Myocardium
,”
Ann. Biomed. Eng.
,
43
(
10
), pp.
2334
2348
.10.1007/s10439-015-1281-z
21.
Avazmohammadi
,
R.
,
Hill
,
M. R.
,
Simon
,
M. A.
,
Zhang
,
W.
, and
Sacks
,
M. S.
,
2017
, “
A Novel Constitutive Model for Passive Right Ventricular Myocardium: Evidence for Myofiber–Collagen Fiber Mechanical Coupling
,”
Biomech. Model. Mechanobiol.
,
16
(
2
), pp.
561
581
.10.1007/s10237-016-0837-7
22.
Hill
,
M. R.
,
Simon
,
M. A.
,
Valdez-Jasso
,
D.
,
Zhang
,
W.
,
Champion
,
H. C.
, and
Sacks
,
M. S.
,
2014
, “
Structural and Mechanical Adaptations of Right Ventricle Free Wall Myocardium to Pressure Overload
,”
Ann. Biomed. Eng.
, 42(12), pp.
2451
2465
.10.1007/s10439-014-1096-3
23.
Guggilam
,
A.
,
Hutchinson
,
K. R.
,
West
,
T. A.
,
Kelly
,
A. P.
,
Galantowicz
,
M. L.
,
Davidoff
,
A. J.
,
Sadayappan
,
S.
, and
Lucchesi
,
P. A.
,
2013
, “
In Vivo and In Vitro Cardiac Responses to Beta-Adrenergic Stimulation in Volume-Overload Heart Failure
,”
J. Mol. Cell. Cardiol.
,
57
, pp.
47
58
.10.1016/j.yjmcc.2012.11.013
24.
McCollum
,
L. T.
,
Gallagher
,
P. E.
, and
Tallant
,
A.
,
2012
, “
Angiotensin-(1-7) Attenuates Angiotensin II-Induced Cardiac Remodeling Associated With Upregulation of Dual-Specificity Phosphatase 1
,”
Am. J. Physiol.: Heart Circ. Physiol.
,
302
(
3
), pp.
801
810
.10.1152/ajpheart.00908.2011
25.
Rockman
,
H. A.
,
Wachhorst
,
S. P.
,
Mao
,
L.
, and
Ross
,
J.
,
1994
, “
ANG II Receptor Blockade Prevents Ventricular Hypertrophy and ANF Gene Expression With Pressure Overload in Mice
,”
Am. J. Physiol.: Hear. Circ. Physiol.
,
266
(
6
), pp.
35
36
.10.1152/ajpheart.1994.266.6.h2468
26.
Yamamoto
,
K.
,
Ohishi
,
M.
,
Katsuya
,
T.
,
Ito
,
N.
,
Ikushima
,
M.
,
Kaibe
,
M.
,
Tatara
,
Y.
,
Shiota
,
A.
,
Sugano
,
S.
,
Takeda
,
S.
,
Rakugi
,
H.
, and
Ogihara
,
T.
,
2006
, “
Deletion of Angiotensin-Converting Enzyme 2 Accelerates Pressure Overload-Induced Cardiac Dysfunction by Increasing Local Angiotensin II
,”
Hypertension
,
47
(
4
), pp.
718
726
.10.1161/01.HYP.0000205833.89478.5b
27.
Burkhoff
,
D.
,
Mirsky
,
I.
, and
Suga
,
H.
,
2005
, “
Assessment of Systolic and Diastolic Ventricular Properties Via Pressure-Volume Analysis: A Guide for Clinical, Translational, and Basic Researchers
,”
Am. J. Physiol.: Heart Circ. Physiol.
,
289
(
2
), pp.
H501
H512
.10.1152/ajpheart.00138.2005
28.
Keshavarz-Motamed
,
Z.
,
Garcia
,
J.
,
Gaillard
,
E.
,
Capoulade
,
R.
,
Le Ven
,
F.
,
Cloutier
,
G.
,
Kadem
,
L.
, and
Pibarot
,
P.
,
2014
, “
Non-Invasive Determination of Left Ventricular Workload in Patients With Aortic Stenosis Using Magnetic Resonance Imaging and Doppler Echocardiography
,”
PLoS One
,
9
(
1
), p.
e86793
.10.1371/journal.pone.0086793
29.
Suga
,
H.
,
Sagawa
,
K.
, and
Shoukas
,
A. A.
,
1973
, “
Load Independence of the Instantaneous Pressure-Volume Ratio of the Canine Left Ventricle and Effects of Epinephrine and Heart Rate on the Ratio
,”
Circ. Res.
,
32
(
3
), pp.
143
150
.10.1161/01.res.32.3.314
30.
Mirsky
,
I.
,
1984
, “
Assessment of Diastolic Function: Suggested Methods and Future Considerations
,”
Circulation
,
69
(
4
), pp.
836
841
.10.1161/01.CIR.69.4.836
31.
Chung
,
C. S.
, and
Granzier
,
H. L.
,
2011
, “
Contribution of Titin and Extracellular Matrix to Passive Pressure and Measurement of Sarcomere Length in the Mouse Left Ventricle
,”
J. Mol. Cell. Cardiol.
,
50
(
4
), pp.
731
739
.10.1016/j.yjmcc.2011.01.005
32.
Cruz Perez
,
B.
,
Tang
,
J.
,
Morris
,
H. J.
,
Palko
,
J. R.
,
Pan
,
X.
,
Hart
,
R. T.
, and
Liu
,
J.
,
2014
, “
Biaxial Mechanical Testing of Posterior Sclera Using High-Resolution Ultrasound Speckle Tracking for Strain Measurements
,”
J. Biomech.
,
47
(
5
), pp.
1151
1156
.10.1016/j.jbiomech.2013.12.009
33.
Khoiy
,
K. A.
,
Pant
,
A. D.
,
Amini
,
R.
, and
Asme
,
M.
,
2018
, “
Quantification of Material Constants for a Phenomenological Constitutive Model of Porcine Tricuspid Valve Leaflets for Simulation Applications
,”
ASME J. Biomech. Eng.
, 140(9), p.
094503
.10.1115/1.4040126
34.
Holzapfel
,
G. A.
,
Gasser
,
T. C.
, and
Ogden
,
R. W.
,
2000
, “
A New Constitutive Framework for Arterial Wall Mechanics and a Comparative Study of Material Models
,”
J. Elast.
,
61
(
1/3
), pp.
1
48
.10.1023/A:1010835316564
35.
Sacks
,
M. S.
,
1999
, “
A Method for Planar Biaxial Mechanical Testing That Includes in-Plane Shear
,”
ASME J. Biomech. Eng.
,
121
(
5
), pp.
551
555
.10.1115/1.2835086
36.
Hutchinson
,
K. R.
,
Stewart
,
J. A.
, and
Lucchesi
,
P. A.
,
2010
, “
Extracellular Matrix Remodeling During the Progression of Volume Overload-Induced Heart Failure
,”
J. Mol. Cell. Cardiol.
,
48
(
3
), pp.
564
569
.10.1016/j.yjmcc.2009.06.001
37.
Dell'italia
,
L. J.
,
Balcells
,
E.
,
Meng
,
Q. C.
,
Su
,
X.
,
Schultz
,
D.
,
Bishop
,
S. P.
,
Machida
,
N.
,
Straeter-Knowlen
,
I. M.
,
Hankes
,
G. H.
,
Dillon
,
R.
,
Cartee
,
R. E.
, and
Oparil
,
S.
,
1997
, “
Volume-Overload Cardiac Hypertrophy is Unaffected by ACE Inhibitor Treatment in Dogs
,”
Am. J. Physiol
,.,
273
(
2
), pp.
H961
H970
.10.1152/ajpheart.1997.273.2.H961
38.
Neves
,
M. F.
,
Amiri
,
F.
,
Virdis
,
A.
,
Diep
,
Q. N.
,
Schiffrin
,
E. L.
,
Neves
,
M. F.
,
Amiri
,
F.
,
Virdis
,
A.
,
Diep
,
Q. N.
, and
Schiffrin
,
E. L.
,
2005
, “
Role of Aldosterone in Angiotensin II-Induced Cardiac and Aortic Inflammation, Fibrosis, and Hypertrophy
,”
Can. J. Physiol. Pharmacol.
,
83
(
11
), pp.
999
1006
.10.1139/y05-068
39.
Engelmayr
,
G. C.
,
Cheng
,
M.
,
Bettinger
,
C. J.
,
Borenstein
,
J. T.
,
Langer
,
R.
, and
Freed
,
L. E.
,
2008
, “
Accordion-Like Honeycombs for Tissue Engineering of Cardiac Anisotropy
,”
Nat. Mater.
,
7
(
12
), pp.
1003
1010
.10.1038/nmat2316
40.
Lee
,
L. C.
,
Ge
,
L.
,
Zhang
,
Z.
,
Pease
,
M.
,
Nikolic
,
S. D.
,
Mishra
,
R.
,
Ratcliffe
,
M. B.
, and
Guccione
,
J. M.
,
2014
, “
Patient-Specific Finite Element Modeling of the Cardiokinetix Parachute(®) Device: Effects on Left Ventricular Wall Stress and Function
,”
Med. Biol. Eng. Comput.
,
52
(
6
), pp.
557
566
.10.1007/s11517-014-1159-5
41.
Kolipaka
,
A.
,
McGee
,
K. P.
,
Araoz
,
P. A.
,
Glaser
,
K. J.
,
Manduca
,
A.
,
Romano
,
A. J.
, and
Ehman
,
R. L.
,
2009
, “
MR Elastography as a Method for the Assessment of Myocardial Stiffness: Comparison With an Established Pressure-Volume Model in a Left Ventricular Model of the Heart
,”
Magn. Reson. Med.
,
62
(
1
), pp.
135
140
.10.1002/mrm.21991
42.
Carabello
,
B. A.
,
Nakano
,
K.
,
Corin
,
W.
,
Biederman
,
R.
, and
Spann
,
J. F.
,
1989
, “
Left Ventricular Function in Experimental Volume Overload Hypertrophy
,”
Am. J. Physiol.: Hear. Circ. Physiol.
,
256
(
4
).
43.
Ruzicka
,
M.
,
Keeley
,
F. W.
, and
Leenen
,
F. H.
,
1994
, “
The Renin-Angiotensin System and Volume Overload-Induced Changes in Cardiac Collagen and Elastin
,”
Circulation
,
90
(
4
), pp.
1989
96
.10.1161/01.CIR.90.4.1989
44.
Yang
,
D.
,
Yuan
,
J.
,
Liu
,
G.
,
Ling
,
Z.
,
Zeng
,
H.
,
Chen
,
Y.
,
Zhang
,
Y.
,
She
,
Q.
, and
Zhou
,
X.
,
2013
, “
Angiotensin Receptor Blockers and Statins Could Alleviate Atrial Fibrosis Via Regulating Platelet-Derived Growth Factor/Rac1/Nuclear Factor-Kappa B Axis
,”
Int. J. Med. Sci.
,
10
(
7
), pp.
812
824
.10.7150/ijms.5931
45.
Kim
,
J. H.
,
Jiang
,
Y.-P.
,
Cohen
,
I. S.
,
Lin
,
R. Z.
, and
Mathias
,
R. T.
,
2017
, “
Pressure-Overload-Induced Angiotensin-Mediated Early Remodeling in Mouse Heart
,”
PLoS One
,
12
(
5
), p.
e0176713
.10.1371/journal.pone.0176713
46.
Regan
,
J. A.
,
Mauro
,
A. G.
,
Carbone
,
S.
,
Marchetti
,
C.
,
Gill
,
R.
,
Mezzaroma
,
E.
,
Valle Raleigh
,
J.
,
Salloum
,
F. N.
,
Van Tassell
,
B. W.
,
Abbate
,
A.
, and
Toldo
,
S.
,
2015
, “
A Mouse Model of Heart Failure With Preserved Ejection Fraction Due to Chronic Infusion of a Low Subpressor Dose of Angiotensin II
,”
Am. J. Physiol.: Circ. Physiol.
,
309
(
5
), pp.
H771
H778
.10.1152/ajpheart.00282.2015
47.
Bacmeister
,
L.
,
Schwarzl
,
M.
,
Warnke
,
S.
,
Stoffers
,
B.
,
Blankenberg
,
S.
,
Westermann
,
D.
, and
Lindner
,
D.
,
2019
, “
Inflammation and Fibrosis in Murine Models of Heart Failure
,”
Basic Res. Cardiol.
,
114
(
3
), pp.
1
35
.10.1007/s00395-019-0722-5
48.
Arora
,
P. D.
,
Narani
,
N.
, and
Mcculloch
,
C. A. G.
,
1999
, “
The Compliance of Collagen Gels Regulates Transforming Growth Factor-? Induction of ⨆-Smooth Muscle Actin in Fibroblasts
,”
Am. J. Pathol.
, 154(3), pp.
871
882
.10.1016/s0002-9440(10)65334-5
49.
Wipff
,
P. J.
,
Rifkin
,
D. B.
,
Meister
,
J. J.
, and
Hinz
,
B.
,
2007
, “
Myofibroblast Contraction Activates Latent TGF-Β1 From the Extracellular Matrix
,”
J. Cell Biol.
,
179
(
6
), pp.
1311
1323
.10.1083/jcb.200704042
50.
Nakamura
,
T.
,
Nakajima
,
T.
,
Suzuki
,
N.
,
Arai
,
S.
, and
Suwa
,
N.
,
1976
, “
Left Ventricular Stiffness and Chamber Geometry in the Pressure-Overloaded Hypertrophied Heart
,”
Tohoku J. Exp. Med.
,
119
(
3
), pp.
245
256
.10.1620/tjem.119.245
51.
Kissling
,
G.
,
Gassenmaier
,
T.
,
Wendt-Gallitelli
,
M. F.
, and
Jacob
,
R.
,
1977
, “
Pressure-Volume Relations, Elastic Modulus, and Contractile Behaviour of the Hypertrophied Left Ventricle of Rats With Goldblatt II Hypertension
,”
Pflügers Arch.-Eur. J. Physiol.
,
369
(
3
), pp.
213
221
.10.1007/BF00582187
52.
Jalil
,
J. E.
,
Doering
,
C. W.
,
Janicki
,
J. S.
,
Pick
,
R.
,
Shroff
,
S. G.
, and
Weber
,
K. T.
,
1989
, “
Fibrillar Collagen and Myocardial Stiffness in the Intact Hypertrophied Rat Left Ventricle
,”
Circ. Res.
,
64
(
6
), pp.
1041
1050
.10.1161/01.res.64.6.1041
53.
Serizawa
,
T.
,
Mirsky
,
I.
,
Carabello
,
B. A.
, and
Grossman
,
W.
,
1982
, “
Diastolic Myocardial Stiffness in Gradually Developing Left Ventricular Hypertrophy in Dog
,”
Am. J. Physiol.: Hear. Circ. Physiol.
,
242
(
4
), pp. H633–H637.10.1152/ajpheart.1982.242.4.H633
54.
Peterson
,
K. L.
,
Tsuji
,
J.
,
Johnson
,
A.
,
DiDonna
,
J.
, and
LeWinter
,
M.
,
1978
, “
Diastolic Left Ventricular Pressure-Volume and Stress-Strain Relations in Patients With Valvular Aortic Stenosis and Left Ventricular Hypertrophy
,”
Circulation
,
58
(
1
), pp.
77
89
.10.1161/01.CIR.58.1.77
55.
Valdez-Jasso
,
D.
,
Simon
,
M. A.
,
Champion
,
H. C.
, and
Sacks
,
M. S.
,
2012
, “
A Murine Experimental Model for the Mechanical Behaviour of Viable Right-Ventricular Myocardium
,”
J. Physiol.
,
590
(
18
), pp.
4571
4584
.10.1113/jphysiol.2012.233015
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