The pathophysiology of heart failure with preserved ejection fraction: From molecular mechanisms to exercise haemodynamics

International Journal of Cardiology

Volumn 158, Issue 3, 2012, Pages 337-343

  Phan, Thanh T ^a   Shivu, Ganesh Nallur ^b   Abozguia, Khalid ^b   Sanderson, John E ^c   Frenneaux, Michael ^b  

^a JAMES COOK UNIVERSITY HOSPITAL   (United Kingdom)

^b UNIVERSITY OF ABERDEEN   (United Kingdom)

^c CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

Author keywords

Diastolic heart failure; Exercise haemodynamics; Hypertrophy; Large artery stiffness; Left ventricular stiffness; Ventricular vascular coupling

Indexed keywords

COLLAGEN TYPE 1; COLLAGEN TYPE 2; COLLAGEN TYPE 3; COLLAGEN TYPE 5; CONNECTIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC GMP DEPENDENT PROTEIN KINASE; DIURETIC AGENT; MATRIX METALLOPROTEINASE; NITRIC OXIDE; TISSUE INHIBITOR OF METALLOPROTEINASE; TROPONIN C; TROPONIN I;

ARTERIAL STIFFNESS; CHRONOTROPISM; CORONARY FLOW RESERVE; DIASTOLIC HEART FAILURE; EXERCISE; EXERCISE TOLERANCE; HEART FAILURE; HEART FAILURE WITH PRESERVED EJECTION FRACTION; HEART HEMODYNAMICS; HEART LEFT VENTRICLE; HEART LEFT VENTRICLE EJECTION FRACTION; HEART LEFT VENTRICLE ENDDIASTOLIC PRESSURE; HEART LEFT VENTRICLE HYPERTROPHY; HEART LEFT VENTRICLE STIFFNESS; HEART MUSCLE COMPLIANCE; HEART MUSCLE FIBROSIS; HEART RATE; HUMAN; HYPERVOLEMIA; LUNG WEDGE PRESSURE; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; TISSUE DOPPLER IMAGING; VASCULAR ENDOTHELIUM; VASODILATATION; CARDIOVASCULAR MORTALITY; CARDIOVASCULAR PARAMETERS; CARDIOVASCULAR RISK; CAUSE OF DEATH; CHRONOTROPIC INCOMPETENCE; CORONARY ARTERY DILATATION; DIASTOLE; DIASTOLIC DYSFUNCTION; DISEASE ASSOCIATION; DRUG MEGADOSE; ELASTANCE STIFFNESS; FLUID INTAKE; HEART FUNCTION; HEART LEFT VENTRICLE CONTRACTILITY; HEART LEFT VENTRICLE OVERLOAD; HEART LEFT VENTRICLE RELAXATION; HEART VENTRICLE ENDDIASTOLIC PRESSURE; HEMODYNAMICS; HYPERTENSION; LEFT VENTRICULAR SYSTOLIC DYSFUNCTION; MOLECULAR BIOLOGY; NONHUMAN; PROGNOSIS; PROTEIN METABOLISM; PULMONARY ARTERY OCCLUSION PRESSURE; SYSTOLIC DYSFUNCTION; VENTRICULAR VASCULAR COUPLING;

EXERCISE; HEART FAILURE; HEMODYNAMICS; HUMANS; HYPERTENSION; HYPERTROPHY, LEFT VENTRICULAR; STROKE VOLUME; VASCULAR STIFFNESS;

EID: 84863633337     PISSN: 01675273     EISSN: 18741754     Source Type: Journal    
DOI: 10.1016/j.ijcard.2011.06.113     Document Type: Review

References (99)

1. W.B. Kannel Incidence and epidemiology of heart failure Heart Fail Rev 5 2 2000 167 173
2. S. Stewart Prognosis of patients with heart failure compared with common types of cancer Heart Fail Monit 3 3 2003 87 94
3. R.S. Vasan, E.J. Benjamin, and D. Levy Prevalence, clinical features and prognosis of diastolic heart failure: an epidemiologic perspective J Am Coll Cardiol 26 7 1995 1565 1574
4. T.E. Owan, D.O. Hodge, R.M. Herges, S.J. Jacobsen, V.L. Roger, and M.M. Redfield Trends in prevalence and outcome of heart failure with preserved ejection fraction N Engl J Med 355 3 2006 251 259
5. R.S. Bhatia, J.V. Tu, and D.S. Lee Outcome of heart failure with preserved ejection fraction in a population-based study N Engl J Med 355 3 2006 260 269
6. M. Klapholz, M. Maurer, and A.M. Lowe New York Heart Failure Consortium. Hospitalization for heart failure in the presence of a normal left ventricular ejection fraction: results of the New York heart failure registry J Am Coll Cardiol 43 8 2004 1432 1438
7. J.B. Somaratne, C. Berry, J.J.V. McMurray, K.K. Poppe, R.N. Doughty, and G.A. Whalley The prognostic significance of heart failure with preserved left ventricular ejection fraction: a literature-based meta-analysis Eur J Heart Fail 11 9 2009 855 862
8. H.S. Lim, R. Beadle, and M. Frenneaux Death and dying in heart failure with normal ejection fraction Am J Cardiol 104 9 2009 1311 1314
9. M.R. Zile, W.H. Gaasch, and I.S. Anand Mode of death in patients with heart failure and a preserved ejection fraction: results from the Irbesartan in heart failure with preserved ejection fraction study (I-Preserve) trial Circulation 121 12 2010 1393 1405
10. M.R. Zile, and D.L. Brutsaert New concepts in diastolic dysfunction and diastolic heart failure: Part I: diagnosis, prognosis, and measurements of diastolic function Circulation 105 11 2002 1387 1393
11. D. Burkhoff, M.S. Maurer, and M. Packer Heart failure with a normal ejection fraction: is it really a disorder of diastolic function? Circulation 107 5 2003 656 658
12. N.P. Nikitin, K.K.A. Witte, A.L. Clark, and J.G.F. Cleland Color tissue Doppler-derived long-axis left ventricular function in heart failure with preserved global systolic function* 1 Am J Cardiol 90 10 2002 1174 1177
13. G. Yip, M. Wang, Y. Zhang, J.W.H. Fung, P.Y. Ho, and J.E. Sanderson Left ventricular long axis function in diastolic heart failure is reduced in both diastole and systole: time for a redefinition? Heart 87 2 2002 121 125
14. T.T. Phan, K. Abozguia, and G.N. Shivu Myocardial contractile inefficiency and dyssynchrony in heart failure with preserved ejection fraction and narrow QRS complex J Am Soc Echocardiogr 23 2 2010 201 206
15. C.M. Yu, Q. Zhang, and G.W. Yip Diastolic and systolic asynchrony in patients with diastolic heart failure: a common but ignored condition J Am Coll Cardiol 49 1 2007 97 105
16. J.E. Sanderson Heart failure with a normal ejection fraction Heart 93 2 2007 155 158
17. G.W. De Keulenaer, and D.L. Brutsaert Systolic and diastolic heart failure: different phenotypes of the same disease? Eur J Heart Fail 9 2 2007 136 143
18. G. Selvetella, E. Hirsch, A. Notte, G. Tarone, and G. Lembo Adaptive and maladaptive hypertrophic pathways: points of convergence and divergence Cardiovasc Res 63 3 2004 373 380
19. M. Sano, and M.D. Schneider Still stressed out but doing fine: normalization of wall stress is superfluous to maintaining cardiac function in chronic pressure overload Circulation 105 1 2002 8 10
20. D. Levy, R.J. Garrison, D.D. Savage, W.B. Kannel, and W.P. Castelli Prognostic implications of echocardiographically determined left ventricular mass in the Framingham Heart Study N Engl J Med 322 22 1990 1561 1566
21. S.F. Vatner, R. Shannon, and L. Hittinger Reduced subendocardial coronary reserve. A potential mechanism for impaired diastolic function in the hypertrophied and failing heart Circulation 81 2 Suppl. 1990
22. J.D. Molkentin, J.R. Lu, and C.L. Antos A calcineurin-dependent transcriptional pathway for cardiac hypertrophy Cell 93 2 1998 215 228
23. Y. Sakata, T. Masuyama, and K. Yamamoto Calcineurin inhibitor attenuates left ventricular hypertrophy, leading to prevention of heart failure in hypertensive rats Circulation 102 18 2000 2269 2275
24. Y. Sakata, T. Masuyama, and K. Yamamoto Renin angiotensin system-dependent hypertrophy as a contributor to heart failure in hypertensive rats: different characteristics from renin angiotensin system-independent hypertrophy J Am Coll Cardiol 37 1 2001 293 299
25. F.M. Fouad, R.C. Tarazi, J.H. Gallagher, W.J. MacIntyre, and S.A. Cook Abnormal left ventricular relaxation in hypertensive patients Clin Sci 59 1980 411 (London, England: 1979)
26. D.W. Kitzman, W.C. Little, and P.H. Brubaker Pathophysiological characterization of isolated diastolic heart failure in comparison to systolic heart failure JAMA 288 17 2002 2144 2150
27. B.H. Lorell, and B.A. Carabello Left ventricular hypertrophy: pathogenesis, detection, and prognosis Circulation 102 4 2000 470 479
28. N. Fukuda, T. Terui, S. Ishiwata, and S. Kurihara Titin-based regulations of diastolic and systolic functions of mammalian cardiac muscle J Mol Cell Cardiol 48 5 2010 876 881
29. T. Masuyama, K. Yamamoto, and Y. Sakata Evolving changes in Doppler mitral flow velocity pattern in rats with hypertensive hypertrophy J Am Coll Cardiol 36 7 2000 2333 2338
30. K. Yamamoto, T. Masuyama, and Y. Sakata Local neurohumoral regulation in the transition to isolated diastolic heart failure in hypertensive heart disease: absence of AT1 receptor downregulation and 'overdrive' of the endothelin system Cardiovasc Res 46 3 2000 421 432
31. K. Yamamoto, T. Masuyama, and Y. Sakata Myocardial stiffness is determined by ventricular fibrosis, but not by compensatory or excessive hypertrophy in hypertensive heart Cardiovasc Res 55 1 2002 76 82
32. G.R. Norton, J. Tsotetsi, B. Trifunovic, C. Hartford, G.P. Candy, and A.J. Woodiwiss Myocardial stiffness is attributed to alterations in cross-linked collagen rather than total collagen or phenotypes in spontaneously hypertensive rats Circulation 96 6 1997 1991 1998
33. J. Diez, A. Panizo, M.J. Gil, I. Monreal, M. Hernandez, and J.P. Mindan Serum markers of collagen type I metabolism in spontaneously hypertensive rats: relation to myocardial fibrosis Circulation 93 5 1996 1026 1032
34. R. Querejeta, B. Lopez, and A. Gonzalez Increased collagen type I synthesis in patients with heart failure of hypertensive origin: relation to myocardial fibrosis Circulation 110 10 2004 1263
35. B. Lopez, A. Gonzalez, N. Varo, C. Laviades, R. Querejeta, and J. Diez Biochemical assessment of myocardial fibrosis in hypertensive heart disease Hypertension 38 5 2001 1222 1226
36. B. Lopez, R. Querejeta, and N. Varo Usefulness of serum carboxy-terminal propeptide of procollagen type I in assessment of the cardioreparative ability of antihypertensive treatment in hypertensive patients Circulation 104 3 2001 286 291
37. S.H. Ahmed, L.L. Clark, and W.R. Pennington Matrix metalloproteinases/ tissue inhibitors of metalloproteinases: relationship between changes in proteolytic determinants of matrix composition and structural, functional, and clinical manifestations of hypertensive heart disease Circulation 113 17 2006 2089
38. R. Martos, J. Baugh, and M. Ledwidge Diastolic heart failure: evidence of increased myocardial collagen turnover linked to diastolic dysfunction Circulation 115 7 2007 888 895
39. S.D. Katz, K. Hryniewicz, and I. Hriljac Vascular endothelial dysfunction and mortality risk in patients with chronic heart failure Circulation 111 3 2005 310 314
40. S.D. Katz, T. Khan, and G.A. Zeballos Decreased activity of the L-ArginineûNitric oxide metabolic pathway in patients with congestive heart failure Circulation 99 16 1999 2113 2117
41. J. Bauersachs, A. Bouloumie, D. Fraccarollo, K. Hu, R. Busse, and G. Ertl Endothelial dysfunction in chronic myocardial infarction despite increased vascular endothelial nitric oxide synthase and soluble guanylate cyclase expression: role of enhanced vascular superoxide production Circulation 100 3 1999 292 298
42. E. Yamamoto, K. Kataoka, and H. Shintaku Novel mechanism and role of angiotensin II induced vascular endothelial injury in hypertensive diastolic heart failure Arterioscler Thromb Vasc Biol 27 12 2007 2569 2575
43. C. Tschope, C.T. Bock, and M. Kasner High prevalence of cardiac parvovirus B19 infection in patients with isolated left ventricular diastolic dysfunction Circulation 111 7 2005 879 886
44. W.G. Hundley, E. Bayram, and C.A. Hamilton Leg flow-mediated arterial dilation in elderly patients with heart failure and normal left ventricular ejection fraction AJP - Heart and Circulatory Physiology 292 3 2007 H1427 H1434
45. L. van Heerebeek, A. Borbely, and H.W. Niessen Myocardial structure and function differ in systolic and diastolic heart failure Circulation 113 16 2006 1966 1973
46. C.C. Lim, and D.B. Sawyer Modulation of cardiac function: titin springs into action J Gen Physiol 125 3 2005 249 252
47. A. Borbely, I. Falcao-Pires, and L. van Heerebeek Hypophosphorylation of the stiff N2B titin isoform raises cardiomyocyte resting tension in failing human myocardium Circ Res 104 6 2009 780 786
48. M. Kruger, S. Kotter, and A. Grutzner Protein kinase G modulates human myocardial passive stiffness by phosphorylation of the titin springs Circ Res 104 1 2009 87 94
49. M.R. Zile, C.F. Baicu, and W.H. Gaasch Diastolic heart failure-abnormalities in active relaxation and passive stiffness of the left ventricle N Engl J Med 350 19 2004 1953 1959
50. D. Westermann, M. Kasner, and P. Steendijk Role of left ventricular stiffness in heart failure with normal ejection fraction Circulation 117 16 2008 2051 2060
51. M.T. Maeder, B.R. Thompson, H.-P. Brunner-La Rocca, and D.M. Kaye Hemodynamic basis of exercise limitation in patients with heart failure and normal ejection fraction J Am Coll Cardiol 56 11 2010 855 863
52. M. Kawaguchi, I. Hay, B. Fetics, and D.A. Kass Combined ventricular systolic and arterial stiffening in patients with heart failure and preserved ejection fraction: implications for systolic and diastolic reserve limitations Circulation 107 5 2003 714 720
53. H. Nonogi, O.M. Hess, M. Ritter, and H.P. Krayenbuehl Diastolic properties of the normal left ventricle during supine exercise Br Heart J 60 1 1988 30 38
54. D.W. Kitzman, M.B. Higginbotham, F.R. Cobb, K.H. Sheikh, and M.J. Sullivan Exercise intolerance in patients with heart failure and preserved left ventricular systolic function: failure of the Frank-Starling mechanism J Am Coll Cardiol 17 5 1991 1065 1072
55. A.F. Leite-Moreira, J. Correia-Pinto, and T.C. Gillebert Afterload induced changes in myocardial relaxation: a mechanism for diastolic dysfunction Cardiovasc Res 43 2 1999 344 353
56. R. Wachter, S. Schmidt-Schweda, and D. Westermann Blunted frequency-dependent upregulation of cardiac output is related to impaired relaxation in diastolic heart failure Eur Heart J 30 24 2009 3027 3036
57. C.P. Liu, C.T. Ting, W. Lawrence, W.L. Maughan, M.S. Chang, and D.A. Kass Diminished contractile response to increased heart rate in intact human left ventricular hypertrophy. Systolic versus diastolic determinants Circulation 88 4 1993 1893 1906
58. H.S. Norman, J. Oujiri, S.J. Larue, C.B. Chapman, K.B. Margulies, and N.K. Sweitzer Decreased cardiac functional reserve in heart failure with preserved systolic function J Card Fail 17 4 2011 301 308
59. T.T. Phan, K. Abozguia, and S.G. Nallur 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 54 5 2009 402 409
60. Y.T. Tan, F. Wenzelburger, and E. Lee The pathophysiology of heart failure with normal ejection fraction: exercise echocardiography reveals complex abnormalities of both systolic and diastolic ventricular function involving torsion, untwist, and longitudinal motion J Am Coll Cardiol 54 1 2009 36 46
61. J. Ross JR., J.W. LINHART, and E. Braunwald Effects of changing heart rate in man by electrical stimulation of the right atrium: studies at rest, during exercise, and with isoproterenol Circulation 32 4 1965 549
62. D.W. Kitzman Diastolic dysfunction: one piece of the heart failure with normal ejection fraction puzzle Circulation 117 16 2008 2044 2046
63. P.V. Ennezat, Y. Lefetz, and S. Marchaux Left ventricular abnormal response during dynamic exercise in patients with heart failure and preserved left ventricular ejection fraction at rest J Card Fail 14 6 2008 475 480
64. J.W. Ha, D. Choi, and S. Park Left ventricular diastolic functional reserve during exercise in patients with impaired myocardial relaxation at rest Heart 95 5 2009 399 404
65. S. Chattopadhyay, M.F. Alamgir, N.P. Nikitin, A.S. Rigby, A.L. Clark, and J.G.F. Cleland Lack of diastolic reserve in patients with heart failure and normal ejection fraction Circ Heart Fail 3 1 2010 35 43
66. T.T. Phan, G.N. Shivu, K. Abozguia, M. Gnanadevan, I. Ahmed, and M. Frenneaux Left ventricular torsion and strain patterns in heart failure with normal ejection fraction are similar to age-related changes Eur J Echocardiogr 10 6 2009 793 800
67. B.A. Borlaug, C.S.P. Lam, V.L. Roger, R.J. Rodeheffer, and M.M. Redfield Contractility and ventricular systolic stiffening in hypertensive heart disease insights into the pathogenesis of heart failure with preserved ejection fraction J Am Coll Cardiol 54 5 2009 410 418
68. B.A. Borlaug, T.P. Olson, and C.S.P. Lam Global cardiovascular reserve dysfunction in heart failure with preserved ejection fraction J Am Coll Cardiol 56 11 2010 845 854
69. J. Wang, K.M. Kurrelmeyer, G. Torre-Amione, and S.F. Nagueh Systolic and diastolic dyssynchrony in patients with diastolic heart failure and the effect of medical therapy J Am Coll Cardiol 49 1 2007 88 96
70. Y.C. Wang, J.J. Hwang, and L.P. Lai Coexistence and exercise exacerbation of intraleft ventricular contractile dyssynchrony in hypertensive patients with diastolic heart failure Am Heart J 154 2 2007 278 284
71. D.A. Kass An epidemic of dyssynchrony: but what does it mean? J Am Coll Cardiol 51 1 2008 12 17
72. T.T. Phan, K. Abozguia, and S.G. Nallur Increased atrial contribution to left ventricular filling compensates for impaired early filling during exercise in heart failure with preserved ejection fraction J Card Fail 15 10 2009 890 897
73. V. Melenovsky, B.A. Borlaug, and B. Rosen 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 49 2 2007 198 207
74. Y.T. Tan, F. Wenzelburger, and E. Lee Reduced left atrial function on exercise in patients with heart failure and normal ejection fraction Heart 96 13 2010 1017 1023
75. W.C. Little, and C.P. Cheng Left ventricular-arterial coupling in conscious dogs Am J Physiol Heart Circ Physiol 261 1 1991 70 76
76. W.C. Little, and C.P. Cheng Effect of exercise on left ventricular-arterial coupling assessed in the pressure-volume plane Am J Physiol Heart Circ Physiol 264 5 1993 1629 1633
77. M. Frenneaux, and L. Williams Ventricular-arterial and ventricular-ventricular interactions and their relevance to diastolic filling Prog Cardiovasc Dis 49 4 2007 252 262
78. C.H. Chen, M. Nakayama, E. Nevo, B.J. Fetics, W.L. Maughan, and D.A. Kass Coupled systolic-ventricular and vascular stiffening with age implications for pressure regulation and cardiac reserve in the elderly J Am Coll Cardiol 32 5 1998 1221 1227
79. C.S.P. Lam, V.L. Roger, and R.J. Rodeheffer Cardiac structure and ventricular-vascular function in persons with heart failure and preserved ejection fraction from Olmsted County, Minnesota Circulation 115 15 2007 1982
80. P.P. De Tombe, S. Jones, D. Burkhoff, W.C. Hunter, and D.A. Kass Ventricular stroke work and efficiency both remain nearly optimal despite altered vascular loading Am J Physiol Heart Circ Physiol 264 6 1993 1817 1824
81. W.G. Hundley, D.W. Kitzman, and T.M. Morgan Cardiac cycle-dependent changes in aortic area and distensibility are reduced in older patients with isolated diastolic heart failure and correlate with exercise intolerance J Am Coll Cardiol 38 3 2001 796 802
82. T.C. Gillebert, A.F. Leite-Moreira, and S.G. De Hert Relaxation-systolic pressure relation. A load-independent assessment of left ventricular contractility Circulation 95 3 1997 745 752
83. J. Ross Jr. Afterload mismatch and preload reserve: a conceptual framework for the analysis of ventricular function Progress Cardiovasc Dis 18 1976 255 264
84. E. Takimoto, D.G. Soergel, P.M. Janssen, L.B. Stull, D.A. Kass, and A.M. Murphy Frequency- and afterload-dependent cardiac modulation in vivo by troponin I with constitutively active protein kinase A phosphorylation sites Circ Res 94 4 2004 496 504
85. R. Zhang, J. Zhao, A. Mandveno, and J.D. Potter Cardiac troponin I phosphorylation increases the rate of cardiac muscle relaxation Circ Res 76 6 1995 1028 1035
86. + - regulatory site of bovine cardiac troponin J Biol Chem 257 1 1982 260 263
87. C.S. Smith, P.A. Bottomley, S.P. Schulman, G. Gerstenblith, and R.G. Weiss Altered creatine kinase adenosine triphosphate kinetics in failing hypertrophied human myocardium Circulation 114 11 2006 1151 1158
88. B.A. Borlaug, V. Melenovsky, and S.D. Russell Impaired chronotropic and vasodilator reserves limit exercise capacity in patients with heart failure and a preserved ejection fraction Circulation 114 20 2006 2138 2147
89. T.T. Phan, G.N. Shivu, and K. Abozguia Impaired heart rate recovery and chronotropic incompetence in patients with heart failure with preserved ejection fraction Circ Heart Fail 3 1 2010 29 34
90. M.S. Maurer, D. Burkhoff, L.P. Fried, J. Gottdiener, D.L. King, and D.W. Kitzman Ventricular structure and function in hypertensive participants with heart failure and a normal ejection fraction: the Cardiovascular Health Study J Am Coll Cardiol 49 9 2007 972 981
91. F. Edelmann, R. Stahrenberg, and G+. Gelbrich Contribution of comorbidities to functional impairment is higher in heart failure with preserved than with reduced ejection fraction Clin Res Cardiol 2011 1 10
92. K.L. He, M. Dickstein, and H.N. Sabbah Mechanisms of heart failure with well preserved ejection fraction in dogs following limited coronary microembolization Cardiovasc Res 64 1 2004 72 83
93. G. Sanjay, J.C. Powers, and N. Abdel-Mohsen The pathogenesis of acute pulmonary edema associated with hypertension N Engl J Med 344 1 2001
94. G. Cotter, M. Metra, O. Milo-Cotter, H.C. Dittrich, and M. Gheorghiade Fluid overload in acute heart failure ΓÇö Re-distribution and other mechanisms beyond fluid accumulation Eur J Heart Fail 10 2 2008 165 169
95. M.S. Maurer, D.L. King, L. El-Khoury Rumbarger, M. Packer, and D. Burkhoff Left heart failure with a normal ejection fraction: identification of different pathophysiologic mechanisms J Card Fail 11 3 2005 177 187
96. J. Adams, G.C. Fonarow, and C.L. Emerman Characteristics and outcomes of patients hospitalized for heart failure in the United States: rationale, design, and preliminary observations from the first 100,000 cases in the Acute Decompensated Heart Failure National Registry (ADHERE) Am Heart J 149 2 2005 209 216
97. G. Cotter, Y. Moshkovitz, and O. Milovanov Acute heart failure: a novel approach to its pathogenesis and treatment Eur J Heart Fail 4 3 2002 227 234
98. G. Cotter, G.M. Felker, K.F. Adams, O. Milo-Cotter, and C.M. O'Connor The pathophysiology of acute heart failure-Is it all about fluid accumulation Am Heart J 155 1 2008 9 18
99. L.G. Shewan, and A.J. Coats Ethics in the authorship and publishing of scientific articles Int J Cardiol 144 2010 1 2