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Published in: Journal of Cardiovascular Magnetic Resonance 1/2017

Open Access 01-12-2016 | Research

Early-stage heart failure with preserved ejection fraction in the pig: a cardiovascular magnetic resonance study

Authors: Ursula Reiter, Gert Reiter, Martin Manninger, Gabriel Adelsmayr, Julia Schipke, Alessio Alogna, Alexandra Rajces, Aurelien F. Stalder, Andreas Greiser, Christian Mühlfeld, Daniel Scherr, Heiner Post, Burkert Pieske, Michael Fuchsjäger

Published in: Journal of Cardiovascular Magnetic Resonance | Issue 1/2017

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Abstract

Background

The hypertensive deoxy-corticosterone acetate (DOCA)-salt-treated pig (hereafter, DOCA pig) was recently introduced as large animal model for early-stage heart failure with preserved ejection fraction (HFpEF). The aim of the present study was to evaluate cardiovascular magnetic resonance (CMR) of DOCA pigs and weight-matched control pigs to characterize ventricular, atrial and myocardial structure and function of this phenotype model.

Methods

Five anesthetized DOCA and seven control pigs underwent 3 T CMR at rest and during dobutamine stress. Left ventricular/atrial (LV/LA) function and myocardial mass (LVMM), strains and torsion were evaluated from (tagged) cine imaging. 4D phase-contrast measurements were used to assess blood flow and peak velocities, including transmitral early-diastolic (E) and myocardial tissue (E’) velocities and coronary sinus blood flow. Myocardial perfusion reserve was estimated from stress-to-rest time-averaged coronary sinus flow. Global native myocardial T1 times were derived from prototype modified Look-Locker inversion-recovery (MOLLI) short-axis T1 maps. After in-vivo measurements, transmural biopsies were collected for stereological evaluation including the volume fractions of interstitium (VV(int/LV)) and collagen (VV(coll/LV)). Rest, stress, and stress-to-rest differences of cardiac and myocardial parameters in DOCA and control animals were compared by t-test.

Results

In DOCA pigs LVMM (p < 0.001) and LV wall-thickness (end-systole/end-diastole, p = 0.003/p = 0.007) were elevated. During stress, increase of LV ejection-fraction and decrease of end-systolic volume accounted for normal contractility reserves in DOCA and control pigs. Rest-to-stress differences of cardiac index (p = 0.040) and end-diastolic volume (p = 0.042) were documented. Maximal (p = 0.042) and minimal (p = 0.012) LA volumes in DOCA pigs were elevated at rest; total LA ejection-fraction decreased during stress (p = 0.006). E’ was lower in DOCA pigs, corresponding to higher E/E’ at rest (p = 0.013) and stress (p = 0.026). Myocardial perfusion reserve was reduced in DOCA pigs (p = 0.031). T1-times and VV(int/LV) did not differ between groups, whereas VV(coll/LV) levels were higher in DOCA pigs (p = 0.044).

Conclusions

LA enlargement, E’ and E/E’ were the markers that showed the most pronounced differences between DOCA and control pigs at rest. Inadequate increase of myocardial perfusion reserve during stress might represent a metrics for early-stage HFpEF. Myocardial T1 mapping could not detect elevated levels of myocardial collagen in this model.

Trial registration

The study was approved by the local Bioethics Committee of Vienna, Austria (BMWF-66.010/0091-II/3b/2013).
Literature
1.
go back to reference Nichols GA, Reynolds K, Kimes TM, Rosales AG, Chan WW. Comparison of risk of Re-hospitalization, all-cause mortality, and medical care resource utilization in patients with heart failure and preserved versus reduced ejection fraction. Am J Cardiol. 2015;116(7):1088–92.PubMedCrossRef Nichols GA, Reynolds K, Kimes TM, Rosales AG, Chan WW. Comparison of risk of Re-hospitalization, all-cause mortality, and medical care resource utilization in patients with heart failure and preserved versus reduced ejection fraction. Am J Cardiol. 2015;116(7):1088–92.PubMedCrossRef
2.
go back to reference Bhatia RS, Tu JV, Lee DS, Austin PC, Fang J, Haouzi A, Gong Y, Liu PP. Outcome of heart failure with preserved ejection fraction in a population-based study. N Engl J Med. 2006;355(3):260–9.PubMedCrossRef Bhatia RS, Tu JV, Lee DS, Austin PC, Fang J, Haouzi A, Gong Y, Liu PP. Outcome of heart failure with preserved ejection fraction in a population-based study. N Engl J Med. 2006;355(3):260–9.PubMedCrossRef
3.
go back to reference Shah AM, Pfeffer MA. The many faces of heart failure with preserved ejection fraction. Nat Rev Cardiol. 2012;9(10):555–6.PubMedCrossRef Shah AM, Pfeffer MA. The many faces of heart failure with preserved ejection fraction. Nat Rev Cardiol. 2012;9(10):555–6.PubMedCrossRef
4.
go back to reference Shah SJ, Katz DH, Selvaraj S, Burke MA, Yancy CW, Gheorghiade M, Bonow RO, Huang CC, Deo RC. Phenomapping for novel classification of heart failure with preserved ejection fraction. Circulation. 2015;131(3):269–79.PubMedCrossRef Shah SJ, Katz DH, Selvaraj S, Burke MA, Yancy CW, Gheorghiade M, Bonow RO, Huang CC, Deo RC. Phenomapping for novel classification of heart failure with preserved ejection fraction. Circulation. 2015;131(3):269–79.PubMedCrossRef
5.
go back to reference Conceicao G, Heinonen I, Lourenco AP, Duncker DJ, Falcao-Pires I. Animal models of heart failure with preserved ejection fraction. Neth Heart J. 2016;24(4):275–86.PubMedPubMedCentralCrossRef Conceicao G, Heinonen I, Lourenco AP, Duncker DJ, Falcao-Pires I. Animal models of heart failure with preserved ejection fraction. Neth Heart J. 2016;24(4):275–86.PubMedPubMedCentralCrossRef
6.
go back to reference Terris JM, Berecek KH, Cohen EL, Stanley JC, Whitehouse Jr WM, Bohr DF. Deoxycorticosterone hypertension in the pig. Clin Sci Mol Med Suppl. 1976;3:303s–5.PubMed Terris JM, Berecek KH, Cohen EL, Stanley JC, Whitehouse Jr WM, Bohr DF. Deoxycorticosterone hypertension in the pig. Clin Sci Mol Med Suppl. 1976;3:303s–5.PubMed
7.
go back to reference Miller 2nd AW, Bohr DF, Schork AM, Terris JM. Hemodynamic responses to DOCA in young pigs. Hypertension. 1979;1(6):591–7.PubMedCrossRef Miller 2nd AW, Bohr DF, Schork AM, Terris JM. Hemodynamic responses to DOCA in young pigs. Hypertension. 1979;1(6):591–7.PubMedCrossRef
8.
go back to reference Cohen DM, Grekin RJ, Mitchell J, Rice WH, Bohr DF. Hemodynamic, endocrine, and electrolyte changes during sodium restriction in DOCA hypertensive pigs. Hypertension. 1980;2(4):490–6.PubMedCrossRef Cohen DM, Grekin RJ, Mitchell J, Rice WH, Bohr DF. Hemodynamic, endocrine, and electrolyte changes during sodium restriction in DOCA hypertensive pigs. Hypertension. 1980;2(4):490–6.PubMedCrossRef
9.
go back to reference Sweadner KJ, Herrera VL, Amato S, Moellmann A, Gibbons DK, Repke KR. Immunologic identification of Na+, K(+)-ATPase isoforms in myocardium. Isoform change in deoxycorticosterone acetate-salt hypertension. Circ Res. 1994;74(4):669–78.PubMedCrossRef Sweadner KJ, Herrera VL, Amato S, Moellmann A, Gibbons DK, Repke KR. Immunologic identification of Na+, K(+)-ATPase isoforms in myocardium. Isoform change in deoxycorticosterone acetate-salt hypertension. Circ Res. 1994;74(4):669–78.PubMedCrossRef
10.
go back to reference Terris JM, Simmonds RC. The Yucatan miniature swine: an improved pig model for the study of desoxycorticosterone-acetate (DOCA) and aldosterone hypertension. Proc Soc Exp Biol Med. 1982;171(1):79–82.PubMedCrossRef Terris JM, Simmonds RC. The Yucatan miniature swine: an improved pig model for the study of desoxycorticosterone-acetate (DOCA) and aldosterone hypertension. Proc Soc Exp Biol Med. 1982;171(1):79–82.PubMedCrossRef
11.
go back to reference Berecek KH, Bohr DF. Structural and functional changes in vascular resistance and reactivity in the deoxycorticosterone acetate (DOCA)-hypertensive pig. Circ Res. 1977;40(5 Suppl 1):I146–52.PubMed Berecek KH, Bohr DF. Structural and functional changes in vascular resistance and reactivity in the deoxycorticosterone acetate (DOCA)-hypertensive pig. Circ Res. 1977;40(5 Suppl 1):I146–52.PubMed
12.
go back to reference Berecek KH, Bohr DF. Whole body vascular reactivity during the development of deoxycorticosterone acetate hypertension in the pig. Circ Res. 1978;42(6):764–71.PubMedCrossRef Berecek KH, Bohr DF. Whole body vascular reactivity during the development of deoxycorticosterone acetate hypertension in the pig. Circ Res. 1978;42(6):764–71.PubMedCrossRef
13.
go back to reference Walterhouse DO, Reinish LW, Mitchell J, Bohr DF. Aortic stiffness in the DOCA-hypertensive pig. Clin Physiol Biochem. 1984;2(4):146–53.PubMed Walterhouse DO, Reinish LW, Mitchell J, Bohr DF. Aortic stiffness in the DOCA-hypertensive pig. Clin Physiol Biochem. 1984;2(4):146–53.PubMed
14.
go back to reference Kamm KE, Gerthoffer WT, Murphy RA, Bohr DF. Mechanical properties of carotid arteries from DOCA hypertensive swine. Hypertension. 1989;13(2):102–9.PubMedCrossRef Kamm KE, Gerthoffer WT, Murphy RA, Bohr DF. Mechanical properties of carotid arteries from DOCA hypertensive swine. Hypertension. 1989;13(2):102–9.PubMedCrossRef
15.
go back to reference Webb RC. Potassium relaxation of vascular smooth muscle from DOCA hypertensive pigs. Hypertension. 1982;4(5):609–19.PubMedCrossRef Webb RC. Potassium relaxation of vascular smooth muscle from DOCA hypertensive pigs. Hypertension. 1982;4(5):609–19.PubMedCrossRef
16.
go back to reference Ciccone CD, Zambraski EJ. Effects of acute renal denervation on kidney function in deoxycorticosterone acetate-hypertensive swine. Hypertension. 1986;8(10):925–31.PubMedCrossRef Ciccone CD, Zambraski EJ. Effects of acute renal denervation on kidney function in deoxycorticosterone acetate-hypertensive swine. Hypertension. 1986;8(10):925–31.PubMedCrossRef
17.
go back to reference Schwarzl M, Hamdani N, Seiler S, Alogna A, Manninger M, Reilly S, Zirngast B, Kirsch A, Steendijk P, Verderber J, Zweiker D, Eller P, Hofler G, Schauer S, Eller K, Maechler H, Pieske BM, Linke WA, Casadei B, Post H. A porcine model of hypertensive cardiomyopathy: implications for heart failure with preserved ejection fraction. Am J Physiol Heart Circ Physiol. 2015;309(9):H1407–18.PubMedCrossRef Schwarzl M, Hamdani N, Seiler S, Alogna A, Manninger M, Reilly S, Zirngast B, Kirsch A, Steendijk P, Verderber J, Zweiker D, Eller P, Hofler G, Schauer S, Eller K, Maechler H, Pieske BM, Linke WA, Casadei B, Post H. A porcine model of hypertensive cardiomyopathy: implications for heart failure with preserved ejection fraction. Am J Physiol Heart Circ Physiol. 2015;309(9):H1407–18.PubMedCrossRef
18.
go back to reference Hunt SA, Abraham WT, Chin MH, Feldman AM, Francis GS, Ganiats TG, Jessup M, Konstam MA, Mancini DM, Michl K, Oates JA, Rahko PS, Silver MA, Stevenson LW, Yancy CW, American College of Cardiology Foundation, American Heart Association. 2009 focused update incorporated into the ACC/AHA 2005 guidelines for the diagnosis and management of heart failure in adults a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines Developed in Collaboration with the International Society for Heart and Lung Transplantation. J Am Coll Cardiol. 2009;53(15):e1–90.PubMedCrossRef Hunt SA, Abraham WT, Chin MH, Feldman AM, Francis GS, Ganiats TG, Jessup M, Konstam MA, Mancini DM, Michl K, Oates JA, Rahko PS, Silver MA, Stevenson LW, Yancy CW, American College of Cardiology Foundation, American Heart Association. 2009 focused update incorporated into the ACC/AHA 2005 guidelines for the diagnosis and management of heart failure in adults a report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines Developed in Collaboration with the International Society for Heart and Lung Transplantation. J Am Coll Cardiol. 2009;53(15):e1–90.PubMedCrossRef
19.
go back to reference Friedrich MG, Bucciarelli-Ducci C, White JA, Plein S, Moon JC, Almeida AG, Kramer CM, Neubauer S, Pennell DJ, Petersen SE, Kwong RY, Ferrari VA, Schulz-Menger J, Sakuma H, Schelbert EB, Larose E, Eitel I, Carbone I, Taylor AJ, Young A, de Roos A, Nagel E. Simplifying cardiovascular magnetic resonance pulse sequence terminology. J Cardiovasc Magn Reson. 2014;16:3960.PubMedPubMedCentralCrossRef Friedrich MG, Bucciarelli-Ducci C, White JA, Plein S, Moon JC, Almeida AG, Kramer CM, Neubauer S, Pennell DJ, Petersen SE, Kwong RY, Ferrari VA, Schulz-Menger J, Sakuma H, Schelbert EB, Larose E, Eitel I, Carbone I, Taylor AJ, Young A, de Roos A, Nagel E. Simplifying cardiovascular magnetic resonance pulse sequence terminology. J Cardiovasc Magn Reson. 2014;16:3960.PubMedPubMedCentralCrossRef
20.
go back to reference Treibel TA, White SK, Moon JC. Myocardial tissue characterization: histological and pathophysiological correlation. Curr Cardiovasc Imaging Rep. 2014;7(3):9254.PubMedPubMedCentralCrossRef Treibel TA, White SK, Moon JC. Myocardial tissue characterization: histological and pathophysiological correlation. Curr Cardiovasc Imaging Rep. 2014;7(3):9254.PubMedPubMedCentralCrossRef
21.
go back to reference McMurray JJ, Adamopoulos S, Anker SD, Auricchio A, Bohm M, Dickstein K, Falk V, Filippatos G, Fonseca C, Gomez-Sanchez MA, Jaarsma T, Kober L, Lip GY, Maggioni AP, Parkhomenko A, Pieske BM, Popescu BA, Ronnevik PK, Rutten FH, Schwitter J, Seferovic P, Stepinska J, Trindade PT, Voors AA, Zannad F, Zeiher A, Task Force for the Diagnosis and Treatment of Acute and Chronic Heart Failure 2012 of the European Society of Cardiology, Bax JJ, Baumgartner H, Ceconi C, Dean V, Deaton C, Fagard R, Funck-Brentano C, Hasdai D, Hoes A, Kirchhof P, Knuuti J, Kolh P, McDonagh T, Moulin C, Popescu BA, Reiner Z, Sechtem U, Sirnes PA, Tendera M, Torbicki A, Vahanian A, Windecker S, McDonagh T, Sechtem U, Bonet LA, Avraamides P, Ben Lamin HA, Brignole M, Coca A, Cowburn P, Dargie H, Elliott P, Flachskampf FA, Guida GF, Hardman S, Iung B, Merkely B, Mueller C, Nanas JN, Nielsen OW, Orn S, Parissis JT, Ponikowski P, ESC Committee for Practice Guidelines. ESC guidelines for the diagnosis and treatment of acute and chronic heart failure 2012: The Task Force for the Diagnosis and Treatment of Acute and Chronic Heart Failure 2012 of the European Society of Cardiology. Developed in collaboration with the Heart Failure Association (HFA) of the ESC. Eur J Heart Fail. 2012;14(8):803–69.PubMedCrossRef McMurray JJ, Adamopoulos S, Anker SD, Auricchio A, Bohm M, Dickstein K, Falk V, Filippatos G, Fonseca C, Gomez-Sanchez MA, Jaarsma T, Kober L, Lip GY, Maggioni AP, Parkhomenko A, Pieske BM, Popescu BA, Ronnevik PK, Rutten FH, Schwitter J, Seferovic P, Stepinska J, Trindade PT, Voors AA, Zannad F, Zeiher A, Task Force for the Diagnosis and Treatment of Acute and Chronic Heart Failure 2012 of the European Society of Cardiology, Bax JJ, Baumgartner H, Ceconi C, Dean V, Deaton C, Fagard R, Funck-Brentano C, Hasdai D, Hoes A, Kirchhof P, Knuuti J, Kolh P, McDonagh T, Moulin C, Popescu BA, Reiner Z, Sechtem U, Sirnes PA, Tendera M, Torbicki A, Vahanian A, Windecker S, McDonagh T, Sechtem U, Bonet LA, Avraamides P, Ben Lamin HA, Brignole M, Coca A, Cowburn P, Dargie H, Elliott P, Flachskampf FA, Guida GF, Hardman S, Iung B, Merkely B, Mueller C, Nanas JN, Nielsen OW, Orn S, Parissis JT, Ponikowski P, ESC Committee for Practice Guidelines. ESC guidelines for the diagnosis and treatment of acute and chronic heart failure 2012: The Task Force for the Diagnosis and Treatment of Acute and Chronic Heart Failure 2012 of the European Society of Cardiology. Developed in collaboration with the Heart Failure Association (HFA) of the ESC. Eur J Heart Fail. 2012;14(8):803–69.PubMedCrossRef
22.
23.
go back to reference Kelley KW, Curtis SE, Marzan GT, Karara HM, Anderson CR. Body surface area of female swine. J Anim Sci. 1973;36(5):927–30.PubMedCrossRef Kelley KW, Curtis SE, Marzan GT, Karara HM, Anderson CR. Body surface area of female swine. J Anim Sci. 1973;36(5):927–30.PubMedCrossRef
24.
go back to reference Schulz-Menger J, Bluemke DA, Bremerich J, Flamm SD, Fogel MA, Friedrich MG, Kim RJ, von Knobelsdorff-Brenkenhoff F, Kramer CM, Pennell DJ, Plein S, Nagel E. Standardized image interpretation and post processing in cardiovascular magnetic resonance: Society for Cardiovascular Magnetic Resonance (SCMR) board of trustees task force on standardized post processing. J Cardiovasc Magn Reson. 2013;15:35.PubMedPubMedCentralCrossRef Schulz-Menger J, Bluemke DA, Bremerich J, Flamm SD, Fogel MA, Friedrich MG, Kim RJ, von Knobelsdorff-Brenkenhoff F, Kramer CM, Pennell DJ, Plein S, Nagel E. Standardized image interpretation and post processing in cardiovascular magnetic resonance: Society for Cardiovascular Magnetic Resonance (SCMR) board of trustees task force on standardized post processing. J Cardiovasc Magn Reson. 2013;15:35.PubMedPubMedCentralCrossRef
25.
go back to reference Lavine SJ. Index of myocardial performance is afterload dependent in the normal and abnormal left ventricle. J Am Soc Echocardiogr. 2005;18(4):342–50.PubMedCrossRef Lavine SJ. Index of myocardial performance is afterload dependent in the normal and abnormal left ventricle. J Am Soc Echocardiogr. 2005;18(4):342–50.PubMedCrossRef
26.
go back to reference Sievers B, Kirchberg S, Addo M, Bakan A, Brandts B, Trappe HJ. Assessment of left atrial volumes in sinus rhythm and atrial fibrillation using the biplane area-length method and cardiovascular magnetic resonance imaging with TrueFISP. J Cardiovasc Magn Reson. 2004;6(4):855–63.PubMedCrossRef Sievers B, Kirchberg S, Addo M, Bakan A, Brandts B, Trappe HJ. Assessment of left atrial volumes in sinus rhythm and atrial fibrillation using the biplane area-length method and cardiovascular magnetic resonance imaging with TrueFISP. J Cardiovasc Magn Reson. 2004;6(4):855–63.PubMedCrossRef
27.
go back to reference Schwitter J, DeMarco T, Kneifel S, von Schulthess GK, Jorg MC, Arheden H, Ruhm S, Stumpe K, Buck A, Parmley WW, Luscher TF, Higgins CB. Magnetic resonance-based assessment of global coronary flow and flow reserve and its relation to left ventricular functional parameters: a comparison with positron emission tomography. Circulation. 2000;101(23):2696–702.PubMedCrossRef Schwitter J, DeMarco T, Kneifel S, von Schulthess GK, Jorg MC, Arheden H, Ruhm S, Stumpe K, Buck A, Parmley WW, Luscher TF, Higgins CB. Magnetic resonance-based assessment of global coronary flow and flow reserve and its relation to left ventricular functional parameters: a comparison with positron emission tomography. Circulation. 2000;101(23):2696–702.PubMedCrossRef
28.
go back to reference Kellman P, Wilson JR, Xue H, Ugander M, Arai AE. Extracellular volume fraction mapping in the myocardium, part 1: evaluation of an automated method. J Cardiovasc Magn Reson. 2012;14:63.PubMedPubMedCentralCrossRef Kellman P, Wilson JR, Xue H, Ugander M, Arai AE. Extracellular volume fraction mapping in the myocardium, part 1: evaluation of an automated method. J Cardiovasc Magn Reson. 2012;14:63.PubMedPubMedCentralCrossRef
29.
go back to reference Konstam MA, Kramer DG, Patel AR, Maron MS, Udelson JE. Left ventricular remodeling in heart failure: current concepts in clinical significance and assessment. JACC Cardiovasc Imaging. 2011;4(1):98–108.PubMedCrossRef Konstam MA, Kramer DG, Patel AR, Maron MS, Udelson JE. Left ventricular remodeling in heart failure: current concepts in clinical significance and assessment. JACC Cardiovasc Imaging. 2011;4(1):98–108.PubMedCrossRef
32.
go back to reference Zile MR, Baicu CF, Ikonomidis JS, Stroud RE, Nietert PJ, Bradshaw AD, Slater R, Palmer BM, Van Buren P, Meyer M, Redfield MM, Bull DA, Granzier HL, LeWinter MM. Myocardial stiffness in patients with heart failure and a preserved ejection fraction: contributions of collagen and titin. Circulation. 2015;131(14):1247–59.PubMedPubMedCentralCrossRef Zile MR, Baicu CF, Ikonomidis JS, Stroud RE, Nietert PJ, Bradshaw AD, Slater R, Palmer BM, Van Buren P, Meyer M, Redfield MM, Bull DA, Granzier HL, LeWinter MM. Myocardial stiffness in patients with heart failure and a preserved ejection fraction: contributions of collagen and titin. Circulation. 2015;131(14):1247–59.PubMedPubMedCentralCrossRef
33.
go back to reference Bull S, White SK, Piechnik SK, Flett AS, Ferreira VM, Loudon M, Francis JM, Karamitsos TD, Prendergast BD, Robson MD, Neubauer S, Moon JC, Myerson SG. Human non-contrast T1 values and correlation with histology in diffuse fibrosis. Heart. 2013;99(13):932–7.PubMedPubMedCentralCrossRef Bull S, White SK, Piechnik SK, Flett AS, Ferreira VM, Loudon M, Francis JM, Karamitsos TD, Prendergast BD, Robson MD, Neubauer S, Moon JC, Myerson SG. Human non-contrast T1 values and correlation with histology in diffuse fibrosis. Heart. 2013;99(13):932–7.PubMedPubMedCentralCrossRef
34.
go back to reference Su MY, Lin LY, Tseng YH, Chang CC, Wu CK, Lin JL, Tseng WY. CMR-verified diffuse myocardial fibrosis is associated with diastolic dysfunction in HFpEF. JACC Cardiovasc Imaging. 2014;7(10):991–7.PubMedCrossRef Su MY, Lin LY, Tseng YH, Chang CC, Wu CK, Lin JL, Tseng WY. CMR-verified diffuse myocardial fibrosis is associated with diastolic dysfunction in HFpEF. JACC Cardiovasc Imaging. 2014;7(10):991–7.PubMedCrossRef
35.
go back to reference Mohammed SF, Hussain S, Mirzoyev SA, Edwards WD, Maleszewski JJ, Redfield MM. Coronary microvascular rarefaction and myocardial fibrosis in heart failure with preserved ejection fraction. Circulation. 2015;131(6):550–9.PubMedCrossRef Mohammed SF, Hussain S, Mirzoyev SA, Edwards WD, Maleszewski JJ, Redfield MM. Coronary microvascular rarefaction and myocardial fibrosis in heart failure with preserved ejection fraction. Circulation. 2015;131(6):550–9.PubMedCrossRef
36.
go back to reference Kato S, Saito N, Kirigaya H, Gyotoku D, Iinuma N, Kusakawa Y, Iguchi K, Nakachi T, Fukui K, Futaki M, Iwasawa T, Kimura K, Umemura S. Impairment of coronary flow reserve evaluated by phase contrast cine-magnetic resonance imaging in patients with heart failure with preserved ejection fraction. J Am Heart Assoc. 2016;5(2):10.1161/JAHA.115.002649. Kato S, Saito N, Kirigaya H, Gyotoku D, Iinuma N, Kusakawa Y, Iguchi K, Nakachi T, Fukui K, Futaki M, Iwasawa T, Kimura K, Umemura S. Impairment of coronary flow reserve evaluated by phase contrast cine-magnetic resonance imaging in patients with heart failure with preserved ejection fraction. J Am Heart Assoc. 2016;5(2):10.​1161/​JAHA.​115.​002649.
37.
go back to reference Borlaug BA, Melenovsky V, Russell SD, Kessler K, Pacak K, Becker LC, Kass DA. Impaired chronotropic and vasodilator reserves limit exercise capacity in patients with heart failure and a preserved ejection fraction. Circulation. 2006;114(20):2138–47.PubMedCrossRef Borlaug BA, Melenovsky V, Russell SD, Kessler K, Pacak K, Becker LC, Kass DA. Impaired chronotropic and vasodilator reserves limit exercise capacity in patients with heart failure and a preserved ejection fraction. Circulation. 2006;114(20):2138–47.PubMedCrossRef
38.
go back to reference Borlaug BA, Jaber WA, Ommen SR, Lam CS, Redfield MM, Nishimura RA. Diastolic relaxation and compliance reserve during dynamic exercise in heart failure with preserved ejection fraction. Heart. 2011;97(12):964–9.PubMedPubMedCentralCrossRef Borlaug BA, Jaber WA, Ommen SR, Lam CS, Redfield MM, Nishimura RA. Diastolic relaxation and compliance reserve during dynamic exercise in heart failure with preserved ejection fraction. Heart. 2011;97(12):964–9.PubMedPubMedCentralCrossRef
39.
go back to reference Kasner M, Sinning D, Burkhoff D, Tschope C. Diastolic pressure-volume quotient (DPVQ) as a novel echocardiographic index for estimation of LV stiffness in HFpEF. Clin Res Cardiol. 2015;104(11):955–63.PubMedCrossRef Kasner M, Sinning D, Burkhoff D, Tschope C. Diastolic pressure-volume quotient (DPVQ) as a novel echocardiographic index for estimation of LV stiffness in HFpEF. Clin Res Cardiol. 2015;104(11):955–63.PubMedCrossRef
40.
go back to reference Kraigher-Krainer E, Shah AM, Gupta DK, Santos A, Claggett B, Pieske B, Zile MR, Voors AA, Lefkowitz MP, Packer M, McMurray JJ, Solomon SD, PARAMOUNT Investigators. Impaired systolic function by strain imaging in heart failure with preserved ejection fraction. J Am Coll Cardiol. 2014;63(5):447–56.PubMedCrossRef Kraigher-Krainer E, Shah AM, Gupta DK, Santos A, Claggett B, Pieske B, Zile MR, Voors AA, Lefkowitz MP, Packer M, McMurray JJ, Solomon SD, PARAMOUNT Investigators. Impaired systolic function by strain imaging in heart failure with preserved ejection fraction. J Am Coll Cardiol. 2014;63(5):447–56.PubMedCrossRef
41.
go back to reference Henein M, Morner S, Lindmark K, Lindqvist P. Impaired left ventricular systolic function reserve limits cardiac output and exercise capacity in HFpEF patients due to systemic hypertension. Int J Cardiol. 2013;168(2):1088–93.PubMedCrossRef Henein M, Morner S, Lindmark K, Lindqvist P. Impaired left ventricular systolic function reserve limits cardiac output and exercise capacity in HFpEF patients due to systemic hypertension. Int J Cardiol. 2013;168(2):1088–93.PubMedCrossRef
42.
go back to reference Wachtell K, Papademetriou V, Smith G, Gerdts E, Dahlof B, Engblom E, Aurigemma GP, Bella JN, Ibsen H, Rokkedal J, Devereux RB. Relation of impaired left ventricular filling to systolic midwall mechanics in hypertensive patients with normal left ventricular systolic chamber function: the Losartan Intervention for Endpoint Reduction in Hypertension (LIFE) study. Am Heart J. 2004;148(3):538–44.PubMedCrossRef Wachtell K, Papademetriou V, Smith G, Gerdts E, Dahlof B, Engblom E, Aurigemma GP, Bella JN, Ibsen H, Rokkedal J, Devereux RB. Relation of impaired left ventricular filling to systolic midwall mechanics in hypertensive patients with normal left ventricular systolic chamber function: the Losartan Intervention for Endpoint Reduction in Hypertension (LIFE) study. Am Heart J. 2004;148(3):538–44.PubMedCrossRef
43.
go back to reference de Simone G, Ganau A, Roman MJ, Devereux RB. Relation of left ventricular longitudinal and circumferential shortening to ejection fraction in the presence or in the absence of mild hypertension. J Hypertens. 1997;15(9):1011–7.PubMedCrossRef de Simone G, Ganau A, Roman MJ, Devereux RB. Relation of left ventricular longitudinal and circumferential shortening to ejection fraction in the presence or in the absence of mild hypertension. J Hypertens. 1997;15(9):1011–7.PubMedCrossRef
44.
go back to reference Aurigemma GP, Silver KH, Priest MA, Gaasch WH. Geometric changes allow normal ejection fraction despite depressed myocardial shortening in hypertensive left ventricular hypertrophy. J Am Coll Cardiol. 1995;26(1):195–202.PubMedCrossRef Aurigemma GP, Silver KH, Priest MA, Gaasch WH. Geometric changes allow normal ejection fraction despite depressed myocardial shortening in hypertensive left ventricular hypertrophy. J Am Coll Cardiol. 1995;26(1):195–202.PubMedCrossRef
45.
go back to reference Melenovsky V, Borlaug BA, Rosen B, Hay I, Ferruci L, Morell CH, Lakatta EG, Najjar SS, Kass DA. Cardiovascular features of heart failure with preserved ejection fraction versus nonfailing hypertensive left ventricular hypertrophy in the urban Baltimore community: the role of atrial remodeling/dysfunction. J Am Coll Cardiol. 2007;49(2):198–207.PubMedCrossRef Melenovsky V, Borlaug BA, Rosen B, Hay I, Ferruci L, Morell CH, Lakatta EG, Najjar SS, Kass DA. Cardiovascular features of heart failure with preserved ejection fraction versus nonfailing hypertensive left ventricular hypertrophy in the urban Baltimore community: the role of atrial remodeling/dysfunction. J Am Coll Cardiol. 2007;49(2):198–207.PubMedCrossRef
46.
go back to reference Yu CM, Lin H, Yang H, Kong SL, Zhang Q, Lee SW. Progression of systolic abnormalities in patients with “isolated” diastolic heart failure and diastolic dysfunction. Circulation. 2002;105(10):1195–201.PubMedCrossRef Yu CM, Lin H, Yang H, Kong SL, Zhang Q, Lee SW. Progression of systolic abnormalities in patients with “isolated” diastolic heart failure and diastolic dysfunction. Circulation. 2002;105(10):1195–201.PubMedCrossRef
47.
go back to reference Kono M, Kisanuki A, Ueya N, Kubota K, Kuwahara E, Takasaki K, Yuasa T, Mizukami N, Miyata M, Tei C. Left ventricular global systolic dysfunction has a significant role in the development of diastolic heart failure in patients with systemic hypertension. Hypertens Res. 2010;33(11):1167–73.PubMedCrossRef Kono M, Kisanuki A, Ueya N, Kubota K, Kuwahara E, Takasaki K, Yuasa T, Mizukami N, Miyata M, Tei C. Left ventricular global systolic dysfunction has a significant role in the development of diastolic heart failure in patients with systemic hypertension. Hypertens Res. 2010;33(11):1167–73.PubMedCrossRef
48.
go back to reference Phan TT, Abozguia K, Nallur Shivu G, Mahadevan G, Ahmed I, Williams L, Dwivedi G, Patel K, Steendijk P, Ashrafian H, Henning A, Frenneaux M. Heart failure with preserved ejection fraction is characterized by dynamic impairment of active relaxation and contraction of the left ventricle on exercise and associated with myocardial energy deficiency. J Am Coll Cardiol. 2009;54(5):402–9.PubMedCrossRef Phan TT, Abozguia K, Nallur Shivu G, Mahadevan G, Ahmed I, Williams L, Dwivedi G, Patel K, Steendijk P, Ashrafian H, Henning A, Frenneaux M. Heart failure with preserved ejection fraction is characterized by dynamic impairment of active relaxation and contraction of the left ventricle on exercise and associated with myocardial energy deficiency. J Am Coll Cardiol. 2009;54(5):402–9.PubMedCrossRef
49.
go back to reference Masuyama T, Lee JM, Nagano R, Nariyama K, Yamamoto K, Naito J, Mano T, Kondo H, Hori M, Kamada T. Doppler echocardiographic pulmonary venous flow-velocity pattern for assessment of the hemodynamic profile in acute congestive heart failure. Am Heart J. 1995;129(1):107–13.PubMedCrossRef Masuyama T, Lee JM, Nagano R, Nariyama K, Yamamoto K, Naito J, Mano T, Kondo H, Hori M, Kamada T. Doppler echocardiographic pulmonary venous flow-velocity pattern for assessment of the hemodynamic profile in acute congestive heart failure. Am Heart J. 1995;129(1):107–13.PubMedCrossRef
50.
go back to reference Barbier P, Solomon S, Schiller NB, Glantz SA. Determinants of forward pulmonary vein flow: an open pericardium pig model. J Am Coll Cardiol. 2000;35(7):1947–59.PubMedCrossRef Barbier P, Solomon S, Schiller NB, Glantz SA. Determinants of forward pulmonary vein flow: an open pericardium pig model. J Am Coll Cardiol. 2000;35(7):1947–59.PubMedCrossRef
52.
go back to reference Burns AT, La Gerche A, MacIsaac AI, Prior DL. Augmentation of left ventricular torsion with exercise is attenuated with age. J Am Soc Echocardiogr. 2008;21(4):315–20.PubMedCrossRef Burns AT, La Gerche A, MacIsaac AI, Prior DL. Augmentation of left ventricular torsion with exercise is attenuated with age. J Am Soc Echocardiogr. 2008;21(4):315–20.PubMedCrossRef
53.
go back to reference Notomi Y, Martin-Miklovic MG, Oryszak SJ, Shiota T, Deserranno D, Popovic ZB, Garcia MJ, Greenberg NL, Thomas JD. Enhanced ventricular untwisting during exercise: a mechanistic manifestation of elastic recoil described by Doppler tissue imaging. Circulation. 2006;113(21):2524–33.PubMedCrossRef Notomi Y, Martin-Miklovic MG, Oryszak SJ, Shiota T, Deserranno D, Popovic ZB, Garcia MJ, Greenberg NL, Thomas JD. Enhanced ventricular untwisting during exercise: a mechanistic manifestation of elastic recoil described by Doppler tissue imaging. Circulation. 2006;113(21):2524–33.PubMedCrossRef
54.
go back to reference Takemoto Y, Barnes ME, Seward JB, Lester SJ, Appleton CA, Gersh BJ, Bailey KR, Tsang TS. Usefulness of left atrial volume in predicting first congestive heart failure in patients > or = 65 years of age with well-preserved left ventricular systolic function. Am J Cardiol. 2005;96(6):832–6.PubMedCrossRef Takemoto Y, Barnes ME, Seward JB, Lester SJ, Appleton CA, Gersh BJ, Bailey KR, Tsang TS. Usefulness of left atrial volume in predicting first congestive heart failure in patients > or = 65 years of age with well-preserved left ventricular systolic function. Am J Cardiol. 2005;96(6):832–6.PubMedCrossRef
55.
go back to reference Paslawska U, Noszczyk-Nowak A, Paslawski R, Janiszewski A, Kiczak L, Zysko D, Nicpon J, Jankowska EA, Szuba A, Ponikowski P. Normal electrocardiographic and echocardiographic (M-mode and two-dimensional) values in Polish Landrace pigs. Acta Vet Scand. 2014;56:54.PubMedPubMedCentralCrossRef Paslawska U, Noszczyk-Nowak A, Paslawski R, Janiszewski A, Kiczak L, Zysko D, Nicpon J, Jankowska EA, Szuba A, Ponikowski P. Normal electrocardiographic and echocardiographic (M-mode and two-dimensional) values in Polish Landrace pigs. Acta Vet Scand. 2014;56:54.PubMedPubMedCentralCrossRef
56.
go back to reference Rienzo M, Bizé A, Pongas D, Michineau S, Melka J, Chan HL, Sambin L, Su JB, Dubois-Randé JL, Hittinger L, Berdeaux A, Ghaleh B. Impaired left ventricular function in the presence of preserved ejection in chronic hypertensive conscious pigs. Basic Res Cardiol. 2012;107:298.PubMedPubMedCentralCrossRef Rienzo M, Bizé A, Pongas D, Michineau S, Melka J, Chan HL, Sambin L, Su JB, Dubois-Randé JL, Hittinger L, Berdeaux A, Ghaleh B. Impaired left ventricular function in the presence of preserved ejection in chronic hypertensive conscious pigs. Basic Res Cardiol. 2012;107:298.PubMedPubMedCentralCrossRef
57.
go back to reference Norman HS, Oujiri J, Larue SJ, Chapman CB, Margulies KB, Sweitzer NK. Decreased cardiac functional reserve in heart failure with preserved systolic function. J Card Fail. 2011;17(4):301–8.PubMedCrossRef Norman HS, Oujiri J, Larue SJ, Chapman CB, Margulies KB, Sweitzer NK. Decreased cardiac functional reserve in heart failure with preserved systolic function. J Card Fail. 2011;17(4):301–8.PubMedCrossRef
Metadata
Title
Early-stage heart failure with preserved ejection fraction in the pig: a cardiovascular magnetic resonance study
Authors
Ursula Reiter
Gert Reiter
Martin Manninger
Gabriel Adelsmayr
Julia Schipke
Alessio Alogna
Alexandra Rajces
Aurelien F. Stalder
Andreas Greiser
Christian Mühlfeld
Daniel Scherr
Heiner Post
Burkert Pieske
Michael Fuchsjäger
Publication date
01-12-2016
Publisher
BioMed Central
Published in
Journal of Cardiovascular Magnetic Resonance / Issue 1/2017
Electronic ISSN: 1532-429X
DOI
https://doi.org/10.1186/s12968-016-0283-9

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