Molecular changes after left ventricular assist device support for heart failure

Circulation Research

Volumn 113, Issue 6, 2013, Pages 777-791

  Birks, Emma J ^a  

^a University of Louisville School of Medicine   (United States)

Author keywords

heart failure; left ventricular assist device; remodeling; reverse remodeling

Indexed keywords

ANTIPORTER; BETA TUBULIN; CALCIUM; CARDIOLIPIN; CLENBUTEROL; CYCLIC AMP; CYTOSKELETON PROTEIN; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; FOLLISTATIN; MITOGEN ACTIVATED PROTEIN KINASE; NEURONAL NITRIC OXIDE SYNTHASE; TISSUE INHIBITOR OF METALLOPROTEINASE 1; TRANSCRIPTION FACTOR NFAT;

ADRENERGIC SYSTEM; APOPTOSIS; ARTICLE; CARDIOMYOPATHY; COLLAGEN METABOLISM; CONGESTIVE CARDIOMYOPATHY; EXCITATION CONTRACTION COUPLING; HEART FAILURE; HEART FUNCTION; HEART LEFT VENTRICLE HYPERTROPHY; HEART MUSCLE; HEART MUSCLE CELL; HEART MUSCLE FIBROSIS; HEART TRANSPLANTATION; HEART VENTRICLE HYPERTROPHY; HETEROTOPIC TRANSPLANTATION; HUMAN; INNATE IMMUNITY; LEFT VENTRICULAR ASSIST DEVICE; NONHUMAN; PRIORITY JOURNAL;

HEART FAILURE; LEFT VENTRICULAR ASSIST DEVICE; REMODELING; REVERSE REMODELING;

ANIMALS; CALCIUM SIGNALING; CYTOSKELETON; EXTRACELLULAR MATRIX; HEART FAILURE; HEART VENTRICLES; HEART-ASSIST DEVICES; HUMANS;

EID: 84883590704     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.113.301413     Document Type: Article

References (100)

1. Braunwald E. Heart failure. J Am Coll Cardiol Heart Failure. 2013;1:1-20.
2. Birks EJ, George RS. Molecular changes occurring during reverse remodelling following left ventricular assist device support. J Cardiovasc Transl Res. 2010;3:635-642.
3. Olivetti G, Capasso JM, Sonnenblick EH, Anversa P. Side-to-side slippage of myocytes participates in ventricular wall remodeling acutely after myocardial infarction in rats. Circ Res. 1990;67:23-34.
4. Narula J, Haider N, Virmani R, DiSalvo TG, Kolodgie FD, Hajjar RJ, Schmidt U, Semigran MJ, Dec GW, Khaw BA. Apoptosis in myocytes in end-stage heart failure. N Engl J Med. 1996;335:1182-1189.
5. Nag AC, Zak R. Dissociation of adult mammalian heart into single cell suspension: an ultrastructural study. J Anat. 1979;129:541-559.
6. Zafeiridis A, Jeevanandam V, Houser SR, Margulies KB. Regression of cellular hypertrophy after left ventricular assist device support. Circulation. 1998;98:656-662.
7. Drakos SG, Kfoury AG, Hammond EH, Reid BB, Revelo MP, Rasmusson BY, Whitehead KJ, Salama ME, Selzman CH, Stehlik J, Clayson SE, Bristow MR, Renlund DG, Li DY. Impact of mechanical unloading on microvasculature and associated central remodeling features of the failing human heart. J Am Coll Cardiol. 2010;56:382-391.
8. Rose AG, Park SJ. Pathology in patients with ventricular assist devices: a study of 21 autopsies, 24 ventricular apical core biopsies and 24 explanted hearts. Cardiovasc Pathol. 2005;14:19-23.
9. Bruckner BA, Stetson SJ, Perez-Verdia A, Youker KA, Radovancevic B, Connelly JH, Koerner MM, Entman ME, Frazier OH, Noon GP, Torre-Amione G. Regression of fibrosis and hypertrophy in failing myocardium following mechanical circulatory support. J Heart Lung Transplant. 2001;20:457-464.
10. Ambardekar AV, Walker JS, Walker LA, Cleveland JC Jr, Lowes BD, Buttrick PM. Incomplete recovery of myocyte contractile function despite improvement of myocardial architecture with left ventricular assist device support. Circ Heart Fail. 2011;4:425-432.
11. Terracciano CM, Hardy J, Birks EJ, Khaghani A, Banner NR, Yacoub MH. Clinical recovery from end-stage heart failure using left-ventricular assist device and pharmacological therapy correlates with increased sarcoplasmic reticulum calcium content but not with regression of cellular hypertrophy. Circulation. 2004;109:2263-2265.
12. Haider N, Arbustini E, Gupta S, Liu H, Narula N, Hajjar R, Moorjani N, Westaby S, Semigran MJ, Dec GW, Chandrashekhar Y, Narula J. Concurrent upregulation of endogenous proapoptotic and antiapoptotic factors in failing human hearts. Nat Clin Pract Cardiovasc Med. 2009;6:250-261.
13. Bartling B, Milting H, Schumann H, Darmer D, Arusoglu L, Koerner MM, El-Banayosy A, Koerfer R, Holtz J, Zerkowski HR. Myocardial gene expression of regulators of myocyte apoptosis and myocyte calcium homeostasis during hemodynamic unloading by ventricular assist devices in patients with end-stage heart failure. Circulation. 1999; 100:II216-II223.
14. Milting H, Bartling B, Schumann H, El-Banayosy A, Wlost S, Rüter F, Darmer D, Holtz J, Körfer R, Zerkowski HR. Altered levels of mRNA of apoptosis-mediating genes after mid-term mechanical ventricular support in dilative cardiomyopathy-first results of the Halle Assist Induced Recovery Study (HAIR). Thorac Cardiovasc Surg. 1999;47:48-50.
15. Chen Y, Park S, Li Y, Missov E, Hou M, Han X, Hall JL, Miller LW, Bache RJ. Alterations of gene expression in failing myocardium following left ventricular assist device support. Physiol Genomics. 2003;14:251-260.
16. Arbustini E, Morbini P, Narula N, et al. Apoptosis in heart failure: abrogation of mitochondrial cytochrome c release after ventricular unloading by LV assist device. Modern Pathology 2001;14:43A (Abstract).
17. Francis GS, Anwar F, Bank AJ, Kubo SH, Jessurun J. Apoptosis, Bcl-2, and proliferating cell nuclear antigen in the failing human heart: observations made after implantation of left ventricular assist device. J Card Fail. 1999;5:308-315.
18. De Jonge, van Wichen DF, van KJ, Kirkels H, Lahpor JR, Gmelig-Meyling FH, van den Tweel JG, de Weger RA. Cardiomyocyte death in patients with end-stage heart failure before and after support with a left ventricular assist device: low incidence of apoptosis despite ubiquitous mediators. J Heart Lung Transplant. 2003;22:1028-1036.
19. Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, Berman K, Cobb MH. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev. 2001;22:153-183.
20. Baba HA, Stypmann J, Grabellus F, Kirchhof P, Sokoll A, Schäfers M, Takeda A, Wilhelm MJ, Scheld HH, Takeda N, Breithardt G, Levkau B. Dynamic regulation of MEK/Erks and Akt/GSK-3beta in human endstage heart failure after left ventricular mechanical support: myocardial mechanotransduction-sensitivity as a possible molecular mechanism. Cardiovasc Res. 2003;59:390-399.
21. Baichwal VR, Baeuerle PA. Activate NF-kappa B or die? Curr Biol. 1997;7:R94-R96.
22. Wohlschlaeger J, Schmitz KJ, Schmid C, Schmid KW, Keul P, Takeda A, Weis S, Levkau B, Baba HA. Reverse remodeling following insertion of left ventricular assist devices (LVAD): a review of the morphological and molecular changes. Cardiovasc Res. 2005;68:376-386.
23. Soppa GK, Barton PJ, Terracciano CM, Yacoub MH. Left ventricular assist device-induced molecular changes in the failing myocardium. Curr Opin Cardiol. 2008;23:206-218.
24. Dipla K, Mattiello JA, Jeevanandam V, Houser SR, Marguiles KB. Myocyte recovery after mechanical support in humans with end-stage heart failure. Circulation.1998;97:2316-2322.
25. Chaudhary KW, Rossman EI, Piacentino V 3rd, Kenessey A, Weber C, Gaughan JP, Ojamaa K, Klein I, Bers DM, Houser SR, Margulies KB. Altered myocardial Ca2+ cycling after left ventricular assist device support in the failing human heart. J Am Coll Cardiol. 2004;44:837-845.
26. Heerdt PM, Klotz S, Burkhoff D. Cardiomyopathic etiology and SERCA2a reverse remodeling during mechanical support of the failing human heart. Anesth Analg. 2006;102:32-37.
27. Terracciano CM, Koban MU, Soppa GK, Siedlecka U, Lee J, Stagg MA, Yacoub MH. The role of the cardiac Na+/Ca2+ exchanger in reverse remodeling: relevance for LVAD-recovery. Ann N Y Acad Sci. 2007;1099:349-360.
28. Ambardekar AV, Buttrick PM. Reverse remodeling with left ventricular assist devices: a review of clinical, cellular, and molecular effects. Circ Heart Fail. 2011;4:224-233.
29. Terracciano CM, Harding SE, Adamson D, Koban M, Tansley P, Birks EJ, Barton PJ, Yacoub MH. Changes in sarcolemmal Ca entry and sarcoplasmic reticulum Ca content in ventricular myocytes from patients with end-stage heart failure following myocardial recovery after combined pharmacological and ventricular assist device therapy. Eur Heart J. 2003;24:1329-1339.
30. Hall JL, Birks EJ, Grindle S, et al. Molecular signature of recovery following combination left ventricular assist device (LVAD) support and pharmacologic therapy. Eur Heart J. 2007;28:613-627.
31. Hall JL, Fermin DR, Birks EJ, Barton PJ, Slaughter M, Eckman P, Baba HA, Wohlschlaeger J, Miller LW. Clinical, molecular, and genomic changes in response to a left ventricular assist device. J Am Coll Cardiol. 2011;57:641-652.
32. Vatta M, Stetson SJ, Perez-Verdia A, Entman ML, Noon GP, Torre-Amione G, Bowles NE, Towbin JA. Molecular remodelling of dystrophin in patients with end-stage cardiomyopathies and reversal in patients on assistance-device therapy. Lancet. 2002;359:936-941.
33. Vatta M, Stetson SJ, Jimenez S, Entman ML, Noon GP, Bowles NE, Towbin JA. Molecular normalization of dystrophin in the failing left and right ventricle of patients treated with either pulsatile or continuous flowtype ventricular devices. J Am Coll Cardiol. 2004;43:811-817.
34. Birks EJ, Hall JL, Barton PJ, Grindle S, Latif N, Hardy JP, Rider JE, Banner NR, Khaghani A, Miller LW, Yacoub MH. Gene profiling changes in cytoskeletal proteins during clinical recovery after left ventricular-assist device support. Circulation. 2005;112:I57-I64.
35. Fatkin D, MacRae C, Saaski T, et al. Missense mutations in the rod domain of the lamin A/C gene as a cause of dilated cardiomyopathy and conduction-system disease. N Engl J Med. 1999;341:1715-1724.
36. Rodrigue-Way A, Burkhoff D, Geesaman BJ, Golden S, Xu J, Pollman MJ, Donoghue M, Jeyaseelan R, Houser S, Breitbart RE, Marks A, Acton S. Sarcomeric genes involved in reverse remodeling of the heart during left ventricular assist device support. J Heart Lung Transplant. 2005;24:73-80.
37. Latif N, Yacoub MH, George R, Barton PJ, Birks EJ. Changes in sarcomeric and non-sarcomeric cytoskeletal proteins and focal adhesion molecules during clinical myocardial recovery after left ventricular assist device support. J Heart Lung Transplant. 2007;26:230-235.
38. de Jonge N, van Wichen DF, Schipper ME, Lahpor JR, Gmelig-Meyling FH, Robles de Medina EO, de Weger RA. Left ventricular assist device in end-stage heart failure: persistence of structural myocyte damage after unloading. An immunohistochemical analysis of the contractile myofilaments. J Am Coll Cardiol. 2002;39:963-969.
39. Akgul A, Skrabal CA, Thompson LO, Loebe M, Lafuente JA, Noon GP, Youker KA. Role of mast cells and their mediators in failing myocardium under mechanical ventricular support. J Heart Lung Transplant. 2004;23:709-715.
40. Bruckner BA, Stetson SJ, Farmer JA, Radovancevic B, Frazier OH, Noon GP, Entman ML, Torre-Amione G, Youker KA. The implications for cardiac recovery of left ventricular assist device support on myocardial collagen content. Am J Surg. 2000;180:498-501; discussion 501.
41. Thompson LO, Skrabal CA, Loebe M, Lafuente JA, Roberts RR, Akgul A, Jones V, Bruckner BA, Thohan V, Noon GP, Youker KA. Plasma neurohormone levels correlate with left ventricular functional and morphological improvement in LVAD patients. J Surg Res. 2005;123:25-32.
42. Klotz S, Foronjy RF, Dickstein ML, Gu A, Garrelds IM, Danser AH, Oz MC, D'Armiento J, Burkhoff D. Mechanical unloading during left ventricular assist device support increases left ventricular collagen cross-linking and myocardial stiffness. Circulation. 2005;112:364-374.
43. Bruggink AH, van Oosterhout MF, de Jonge N, Ivangh B, van Kuik J, Voorbij RH, Cleutjens JP, Gmelig-Meyling FH, de Weger RA. Reverse remodeling of the myocardial extracellular matrix after prolonged left ventricular assist device support follows a biphasic pattern. J Heart Lung Transplant. 2006;25:1091-1098.
44. Li YY, Feng Y, McTiernan CF, Pei W, Moravec CS, Wang P, Rosenblum W, Kormos RL, Feldman AM. Downregulation of matrix metalloproteinases and reduction in collagen damage in the failing human heart after support with left ventricular assist devices. Circulation. 2001;104:1147-1152.
45. Madigan JD, Barbone A, Choudhri AF, Morales DL, Cai B, Oz MC, Burkhoff D. Time course of reverse remodeling of the left ventricle during support with a left ventricular assist device. J Thorac Cardiovasc Surg. 2001;121:902-908.
46. Drakos SG, Kfoury AG, Selzman CH, Verma DR, Nanas JN, Li DY, Stehlik J. Left ventricular assist device unloading effects on myocardial structure and function: current status of the field and call for action. Curr Opin Cardiol. 2011;26:245-255.
47. Birks EJ, Tansley PD, Hardy J, George RS, Bowles CT, Burke M, Banner NR, Khaghani A, Yacoub MH. Left ventricular assist device and drug therapy for the reversal of heart failure. N Engl J Med. 2006;355:1873-1884.
48. Klotz S, Danser AH, Foronjy RF, Oz MC, Wang J, Mancini D, D'Armiento J, Burkhoff D. The impact of angiotensin-converting enzyme inhibitor therapy on the extracellular collagen matrix during left ventricular assist device support in patients with end-stage heart failure. J Am Coll Cardiol. 2007;49:1166-1174.
49. Milting H, Kassner A, Arusoglu L, Meyer HE, Morshuis M, Brendel R, Klauke B, El Banayosy A, Körfer R. Influence of ACE-inhibition and mechanical unloading on the regulation of extracellular matrix proteins in the myocardium of heart transplantation candidates bridged by ventricular assist devices. Eur J Heart Fail. 2006;8:278-283.
50. Li YY, Feldman AM, Sun Y, McTiernan CF. Differential expression of tissue inhibitors of metalloproteinases in the failing human heart. Circulation. 1998;98:1728-1734.
51. Barton PJ, Birks EJ, Felkin LE, Cullen ME, Koban MU, Yacoub MH. Increased expression of extracellular matrix regulators TIMP1 and MMP1 in deteriorating heart failure. J Heart Lung Transplant. 2003;22: 738-744.
52. Felkin LE, Birks EJ, George R, Wong S, Khaghani A, Yacoub MH, Barton PJ. A quantitative gene expression profile of matrix metalloproteinases (MMPS) and their inhibitors (TIMPS) in the myocardium of patients with deteriorating heart failure requiring left ventricular assist device support. J Heart Lung Transplant. 2006;25:1413-1419.
53. Felkin LE, Lara-Pezzi E, George R, Yacoub MH, Birks EJ, Barton PJ. Expression of extracellular matrix genes during myocardial recovery from heart failure following left ventricular assist device (LVAD) support. J Heart Lung Transplant 2009;28:117-122.
54. Segura AM, Frazier OH, Demirozu Z, Buja LM. Histopathologic correlates of myocardial improvement in patients supported by a left ventricular assist device. Cardiovasc Pathol. 2011;20:139-145.
55. Segura AM, Barton PJ, George R, Buja LM, Frazier OH, Birks EJ. Correlation of fibrosis and hypertrophy with myocardial improvement during left ventricular assist device (LVAD) support. J Heart Lung Transplant 2011;30:S77.
56. Bruckner BA, Razeghi P, Stetson S, Thompson L, Lafuente J, Entman M, Loebe M, Noon G, Taegtmeyer H, Frazier OH, Youker K. Degree of cardiac fibrosis and hypertrophy at time of implantation predicts myocardial improvement during left ventricular assist device support. J Heart Lung Transplant. 2004;23:36-42.
57. Yamada Y, Saito S, Nishinaka T, Yamazaki K. Myocardial size and fibrosis changes during left ventricular assist device support. ASAIO J. 2012;58:402-406.
58. Ashrafian H, Frenneaux MP, Opie LH. Metabolic mechanisms in heart failure. Circulation. 2007;116:434-448.
59. Lee SH, Doliba N, Osbakken M, Oz M, Mancini D. Improvement of myocardial mitochondrial function after hemodynamic support with left ventricular assist devices in patients with heart failure. J Thorac Cardiovasc Surg. 1998;116:344-349.
60. Heerdt PM, Schlame M, Jehle R, Barbone A, Burkhoff D, Blanck TJ. Disease-specific remodeling of cardiac mitochondria after a left ventricular assist device. Ann Thorac Surg. 2002;73:1216-1221.
61. Mital S, Loke KE, Addonizio LJ, Oz MC, Hintze TH. Left ventricular assist device implantation augments nitric oxide dependent control of mitochondrial respiration in failing human hearts. J Am Coll Cardiol. 2000;36:1897-1902.
62. Razeghi P, Young ME, Ying J, Depre C, Uray IP, Kolesar J, Shipley GL, Moravec CS, Davies PJ, Frazier OH, Taegtmeyer H. Downregulation of metabolic gene expression in failing human heart before and after mechanical unloading. Cardiology. 2002;97:203-209.
63. Nascimben L, Ingwall JS, Pauletto P, Friedrich J, Gwathmey JK, Saks V, Pessina AC, Allen PD. Creatine kinase system in failing and nonfailing human myocardium. Circulation. 1996;94:1894-1901.
64. Cullen ME, Yuen AH, Felkin LE, Smolenski RT, Hall JL, Grindle S, Miller LW, Birks EJ, Yacoub MH, Barton PJ. Myocardial expression of the arginine:glycine amidinotransferase gene is elevated in heart failure and normalized after recovery: potential implications for local creatine synthesis. Circulation. 2006;114:I16-I20.
65. Mann DL, Young JB. Basic mechanisms in congestive heart failure. Recognizing the role of proinflammatory cytokines. Chest. 1994;105:897-904.
66. Birks EJ, Felkin LE, Banner NR, Khaghani A, Barton PJ, Yacoub MH. Increased toll-like receptor 4 in the myocardium of patients requiring left ventricular assist devices. J Heart Lung Transplant. 2004;23:228-235.
67. Birks EJ, Latif N, Owen V, Bowles C, Felkin LE, Mullen AJ, Khaghani A, Barton PJ, Polak JM, Pepper JR, Banner NR, Yacoub MH. Quantitative myocardial cytokine expression and activation of the apoptotic pathway in patients who require left ventricular assist devices. Circulation. 2001;104:I233-I240.
68. Birks EJ, Khaghani A, Bowles C, Hunt D, Pepper JP, Banner NR, Yacoub MH. Serum cytokines in LVAD candidates. Transplantation Proc. 2001;33:1974-1975.
69. Torre-Amione G, Stetson SJ, Youker KA, Durand JB, Radovancevic B, Delgado RM, Frazier OH, Entman ML, Noon GP. Decreased expression of tumor necrosis factor-alpha in failing human myocardium after mechanical circulatory support: a potential mechanism for cardiac recovery. Circulation. 1999;100:1189-1193.
70. Razeghi P, Mukhopadhyay M, Myers TJ, Williams JN, Moravec CS, Frazier OH, Taegtmeyer H. Myocardial tumor necrosis factor-alpha expression does not correlate with clinical indices of heart failure in patients on left ventricular assist device support. Ann Thorac Surg. 2001;72:2044-2050.
71. Harrison CA, Gray PC, Vale WW, Robertson DM. Antagonists of activin signaling: mechanisms and potential biological applications. Trends Endocrinol Metab. 2005;16:73-78.
72. Lara-Pezzi E, Felkin LE, Birks EJ, Sarathchandra P, Panse KD, George R, Hall JL, Yacoub MH, Rosenthal N, Barton PJ. Expression of follistatin-related genes is altered in heart failure. Endocrinology. 2008;149:5822-5827.
73. Haider N, Baliga RR, Chandrashekhar Y, Narula J. Adrenergic excess, hNET1 down-regulation, and compromised mIBG uptake in heart failure poverty in the presence of plenty. J Am Coll Cardiol Cardiovasc Imaging. 2010;3:71-75.
74. Drakos SH, Terrovitis JV, Nanas JN, Charitos EI, Ntalianis AS, Malliaras KG, Diakos N, Koudoumas D, Theodoropoulos S, Yacoub MH, Anastasiou-Nana MI. Reverse electrophysiologic remodeling after cardiac mechanical unloading for end-state nonischemic cardiomyopathy. Ann Thorac Surg. 2011;91:764-769.
75. George RS, Birks EJ, Cheetham A, Webb C, Smolenski RT, Khaghani A, Yacoub MH, Kelion A. The effect of long-term left ventricular assist device support on myocardial sympathetic activity in patients with non-ischaemic dilated cardiomyopathy. Eur J Heart Fail. 2013 Apr 2 [Epub ahead of print].
76. Wohlschlaeger J, Levkau B, Takeda A, Takeda N, Stypmann J, Schmid C, Milting H, Schmid KW, Baba HA. Increase of ABCG2/BCRP+ side population stem cells in myocardium after ventricular unloading. J Heart Lung Transplant. 2012;31:318-324.
77. Rakusan K, Heron MI, Kolar F, Korecky B. Transplantation-induced atrophy of normal and hypertrophic rat hearts: effect on cardiac myocytes and capillaries. J Mol Cell Cardiol. 1997;29:1045-1054.
78. Kinoshita M, Takano H, Takaichi S, Taenaka Y, Nakatani T. Influence of prolonged ventricular assistance on myocardial histopathology in intact heart. Ann Thorac Surg. 1996;61:640-645.
79. Soppa GK, Lee J, Stagg MA, Siedlecka U, Youssef S, Yacoub MH, Terracciano CM. Prolonged mechanical unloading reduces myofilament sensitivity to calcium and sarcoplasmic reticulum calcium uptake leading to contractile dysfunction. J Heart Lung Transplant. 2008;27:882-889.
80. Xydas S, Rosen RS, Ng C, Mercando M, Cohen J, DiTullio M, Magnano A, Marboe CC, Mancini DM, Naka Y, Oz MC, Maybaum S. Mechanical unloading leads to echocardiographic, electrocardiographic, neurohormonal, and histologic recovery. J Heart Lung Transplant. 2006;25:7-15.
81. Ogletree ML, Sweet WE, Talerico C, Klecka ME, Young JB, Smedira NG, Starling RC, Moravec CS. Duration of left ventricular assist device support: effects on abnormal calcium cycling and functional recovery in the failing human heart. J Heart Lung Transplant. 2010;29:554-561.
82. Ibrahim M, Al Masri A, Navaratnarajah M, Siedlecka U, Soppa GK, Moshkov A, Al-Saud SA, Gorelik J, Yacoub MH, Terracciano CM. Prolonged mechanical unloading affects cardiomyocyte excitationcontraction coupling, transverse-tubule structure, and the cell surface. FASEB J. 2010;24:3321-3329.
83. Birks EJ, Miller LW. Myocardial recovery with the use of ventricular assist devices, mechanical circulatory support. 1st ed. A Companion to Braunwald's Heart Disease. Philadelphia, PA: Elsevier Sanders. 2012; p 220-238.
84. Scheuer J, Buttrick P. The cardiac hypertrophic responses to pathologic and physiologic loads. Circulation. 1987;75:I63-I68.
85. Petrou M, Wynne DG, Boheler KR, Yacoub MH. Clenbuterol induces hypertrophy of the latissimus dorsi muscle and heart in the rat with molecular and phenotypic changes. Circulation. 1995;92:II483-II489.
86. Wong K, Boheler KR, Bishop J, Petrou M, Yacoub MH. Clenbuterol induces cardiac hypertrophy with normal functional, morphological and molecular features. Cardiovasc Res. 1998;37:115-122.
87. Soppa GK, Smolenski RT, Latif N, Yuen AH, Malik A, Karbowska J, Kochan Z, Terracciano CM, Yacoub MH. Effects of chronic administration of clenbuterol on function and metabolism of adult rat cardiac muscle. Am J Physiol Heart Circ Physiol. 2005;288:H1468-H1476.
88. Frazier OH, Radovancevic B, Abou-Awdi NL, et al. Ventricular remodelling after prolonged ventricular unloading "heart rest" experience with the heartmate left ventricular assist device. J Heart Lung Transplant. 1994;13(Pt 2):77.
89. Levin HR, Oz MC, Chen JM, Packer M, Rose EA, Burkhoff D. Reversal of chronic ventricular dilation in patients with end-stage cardiomyopathy by prolonged mechanical unloading. Circulation. 1995;91:2717-2720.
90. Frazier OH, Myers TJ. Left ventricular assist system as a bridge to myocardial recovery. Ann Thorac Surg. 1999;68:734-741.
91. Mancini DM, Beniaminovitz A, Levin H, Catanese K, Flannery M, DiTullio M, Savin S, Cordisco ME, Rose E, Oz M. Low incidence of myocardial recovery after left ventricular assist device implantation in patients with chronic heart failure. Circulation. 1998;98:2383-2389.
92. Farrar DJ, Holman WR, McBride LR, Kormos RL, Icenogle TB, Hendry PJ, Moore CH, Loisance DY, El-Banayosy A, Frazier H. Long-term follow-up of Thoratec ventricular assist device bridge-to-recovery patients successfully removed from support after recovery of ventricular function. J Heart Lung Transplant. 2002;21:516-521.
93. Simon MA, Kormos RL, Murali S, Nair P, Heffernan M, Gorcsan J, Winowich S, McNamara DM. Myocardial recovery using ventricular assist devices: prevalence, clinical characteristics, and outcomes. Circulation. 2005;112:I32-I36.
94. Müller J, Wallukat G, Weng YG, Dandel M, Spiegelsberger S, Semrau S, Brandes K, Theodoridis V, Loebe M, Meyer R, Hetzer R. Weaning from mechanical cardiac support in patients with idiopathic dilated cardiomyopathy. Circulation. 1997;96:542-549.
95. Dandel M, Weng Y, Siniawski H, Potapov E, Lehmkuhl HB, Hetzer R. Long-term results in patients with idiopathic dilated cardiomyopathy after weaning from left ventricular assist devices. Circulation. 2005;112:I37-I45.
96. Dandel M, Weng Y, Siniawski H, Potapov E, Drews T, Lehmkuhl HB, Knosalla C, Hetzer R. Prediction of cardiac stability after weaning from left ventricular assist devices in patients with idiopathic dilated cardiomyopathy. Circulation. 2008;118:S94-S105.
97. Maybaum S, Mancini D, Xydas S, Starling RC, Aaronson K, Pagani FD, Miller LW, Margulies K Cardiac improvement during mechanical circulatory support a prospective multicentre study of the LVAD Working group. Circulation. 2007;115:2497-2505.
98. Birks EJ, George RS, Hedger M, Bahrami T, Wilton P, Bowles CT, Webb C, Bougard R, Amrani M, Yacoub MH, Dreyfus G, Khaghani A. Reversal of severe heart failure with a continuous-flow left ventricular assist device and pharmacological therapy: a prospective study. Circulation. 2011;123:381-390.
99. George RS, Sabharwal NK, Webb C, Yacoub MH, Bowles CT, Hedger M, Khaghani A, Birks EJ. Echocardiographic assessment of flow across continuous-flow ventricular assist devices at low speeds. J Heart Lung Transplant. 2010;29:1245-1252.
100. George RS, Yacoub MH, Bowles CT, Hipkin M, Rogers P, Hallas C, Banner NR, Dreyfus G, Khaghani A, Birks EJ. Quality of life after removal of left ventricular assist device for myocardial recovery. J Heart Lung Transplant. 2008;27:165-172.