European Journal of Applied Physiology

, Volume 90, Issue 3–4, pp 250–259

Exercise after heart transplantation

Review Article

Abstract

Exercise intolerance in heart transplant recipients (HTR) has a multifactorial origin, involving complex interactions among cardiac, neurohormonal, vascular, skeletal muscle and pulmonary abnormalities. However, the role of these abnormalities may differ as a function of time after transplantation and of many other variables. The present review is aimed at evaluating the role of cardiac, pulmonary and muscular factors in limiting maximal aerobic performance of HTR, and the benefits of chronic exercise. Whereas pulmonary function does not seem to affect gas exchange until a critical value of diffusing lung capacity is attained, cardiac and skeletal muscle function deterioration may represent relevant factors limiting maximal and submaximal aerobic performance. Cardiac function is mainly limited by chronotropic incompetence and diastolic dysfunction, whereas muscle activity seems to be limited by impaired oxygen supply as a consequence of the reduced capillary network. The latter may be due to either immunosuppressive regimen or deconditioning. Endurance and strength training may greatly improve muscle function and maximal aerobic performance of HTR, and may also reduce side effects of immunosuppressive therapy and control risk factors for cardiac allograft vasculopathy. For the above reasons exercise should be considered an important therapeutic tool in the long-term treatment of heart transplant recipients.

Keywords

Heart transplantation Exercise Cardiac function Muscle function Endurance training 

References

  1. Al-Rawas OA, Carter R, Richens D, Stevenson RD, Naik SK, Tweddel A, Wheatley DJ (1995) Ventilatory and gas exchange abnormalities in chronic heart failure. Eur Respir J 8:2022–2028CrossRefPubMedGoogle Scholar
  2. Al-Rawas OA, Carter R, Stevenson RD, Naik SK, Wheatley DJ (1997) The time course of pulmonary transfer factor changes following heart transplantation Eur J Cardiothorac Surg 12:471–479CrossRefGoogle Scholar
  3. Al-Rawas OA, Carter R, Stevenson RD, Naik SK, Wheatley DJ (2000) Exercise intolerance following heart transplantation. The role of pulmonary diffusing capacity. Chest 118:1661–1670CrossRefPubMedGoogle Scholar
  4. Aranda JM Jr, Hill J (2000) Cardiac transplant vasculopathy. Chest 118:1792–1800CrossRefPubMedGoogle Scholar
  5. Banner NR, Lloyd MH, Hamilton RD, Innes JA, Guz A, Jacoub MH (1989a) Cardiopulmonary response to dynamic exercise after heart and combined heart–lung transplantation. Br Heart J 61:215–223PubMedGoogle Scholar
  6. Banner NR, Patel N, Cox AP, Patton HE, Lachno DR, Jacoub MH (1989b) Altered sympathoadrenal response to dynamic exercise in cardiac transplant recipients. Cardiovasc Res 23:965–972Google Scholar
  7. Beck W, Barnard CN, Schrire V (1969) Heart rate after cardiac transplantation. Circulation 40:437–445PubMedGoogle Scholar
  8. Bengel FM, Ueberfuhr P, Ziegler SI, Nekolla S, Reichart B, Schwaiger M (1999) Serial assessment of sympathetic reinnervation after orthotopic heart transplantation: a longitudinal study using PET and C-11 hydroxyephedrine. Circulation 99:1866–1871PubMedGoogle Scholar
  9. Beniaminovitz A, Coromilas J, Oz M, Galantowicz M, Donchez L, Mancini D (1998) Electrical connection of native and transplanted sinus nodes via atrial pacing improves exercise performance after cardiac transplantation. Am J Cardiol 81:1373–1377CrossRefPubMedGoogle Scholar
  10. Berkenboom G, Crasset V, Giot C, Unger P, Vachiery J, Leclerc J (1998) Endothelial function of internal mammary artery in patients with coronary artery disease and in transplant recipients. Am Heart J 135:488–494PubMedGoogle Scholar
  11. Bernardi L, Valenti C, Wdowczyck-Susic J, Frey AW, Rinaldi M, Spadacini G, Passino C, Martinelli L, Viganò M, Finardi G (1998) Influence of type of surgery on the occurrence of parasympathetic reinnervation after cardiac transplantation. Circulation 97:1368–1374PubMedGoogle Scholar
  12. Bhatia SJ, Kirshenbaum JM, Shemin RJ, Cohn LH, Collins JJ, Di Sesa VJ, Young PJ, Mudge GH Jr, Sutton MG (1987) Time course of resolution of pulmonary hypertension and right ventricular remodelling after orthotopic cardiac transplantation. Circulation 76:819–826PubMedGoogle Scholar
  13. Biring MS, Fournier M, Ross DJ, Lewis MI (1998) Cellular adaptations of skeletal muscles to cyclosporin. J Appl Physiol 84:1967–1975PubMedGoogle Scholar
  14. Boucek MM, Edwards LB, Keck BM, Trulock EP, Taylor DO, Mohacsi PJ, Hertz MI (2002) The registry of the international society of heart and lung transplantation: fifth official pediatric report-2001 to 2002. J Heart Lung Transplant 21:827–840CrossRefPubMedGoogle Scholar
  15. Braith RW, Wood CE, Limacher MC, Pollock ML, Lowenthal DT, Phillis MI, Staples ED (1992) Abnormal neuroendocrine responses during exercise in heart transplant recipients. Circulation 86:1453–1463PubMedGoogle Scholar
  16. Braith RW, Limacher MC, Leggett SH, Pollock ML (1993a) Skeletal muscle strength in heart transplant recipients. J Heart Lung Transplant 12:1018–1023PubMedGoogle Scholar
  17. Braith RW, Limacher MC, Mills RM Jr, Leggett SH, Pollock ML, Staples ED (1993b) Exercise-induced hypoxemia in heart transplant recipients. J Am Coll Cardiol 22:768–776Google Scholar
  18. Braith RW, Plunkett MB, Mills RM Jr (1998a) Cardiac output responses during exercise in volume-expanded heart transplant recipients. Am J Cardiol 81:1152–1156CrossRefPubMedGoogle Scholar
  19. Braith RW, Welsch MA, Mills RM Jr, Keller JW, Pollock ML (1998b) Resistance exercise prevents glucocorticoid-induced myopathy in heart transplant recipients. Med Sci Sports Exerc 30:483–489PubMedGoogle Scholar
  20. Brubaker PH, Berry MJ, Brozena SC, Morley DL, Walter JD, Paolone AP, Bove AA (1993) Relationship of lactate and ventilatory thresholds in cardiac transplant patients. Med Sci Sports Exerc 25:191–196PubMedGoogle Scholar
  21. Bussières LM, Pflugfelder PW, Taylor AW, Noble EG, Kostuk WJ (1997) Changes in skeletal muscle morphology and biochemistry after cardiac transplantation. Am J Cardiol 78:630–634Google Scholar
  22. Calzolari A, Pastore E, Attias L, Cicini P, Giordano U, Parisi F, Ragonese P, Squitieri C, Turchetta A (1998) Cardiorespiratory functional assessment in young heart transplant recipients. Int J Sports Cardiol 7:107–111Google Scholar
  23. Carù B, Bonelli R, Pedretti R, Anza C, Colombo E, Santoro F, La Porta A, Maslowsky F, Marconi C, Cerretelli P (1992) Exercise training in heart transplantation. In: Carù B, Rampulla B, Fracchia G, Tramarin E (eds) Cardiopulmonary rehabilitation. Springer, Berlin Heidelberg New York, pp 119–128Google Scholar
  24. Cerretelli P, Grassi B, Colombini A, Carù B, Marconi C (1988) Gas exchange and metabolic transients in heart transplant recipients. Respir Physiol 74:355–371Google Scholar
  25. Cerretelli P, Marconi C, Meyer M, Ferretti G, Grassi B (1992) Gas exchange kinetics in heart transplant recipients. Chest 101:199S-205SPubMedGoogle Scholar
  26. Christos SC, Katch V, Crowley DC, Eakin BL, Lindauer AL, Beekman RH (1992) Hemodynamic responses to upright exercise of adolescent cardiac transplant recipients. J Pediatr 121:312–316PubMedGoogle Scholar
  27. Daida H, Squires RW, Allison TG, Johnson BD, Gau G ( 1996) Sequential assessment of exercise tolerance in heart transplantation compared with coronary artery bypass surgery after phase II cardiac rehabilitation. Am J Cardiol 77:696–700CrossRefPubMedGoogle Scholar
  28. De Groot-Kruseman HA, Baan CC, Hagman EM, Mol WM, Niesters HG, Maat AP, Vantrimpont PJ, Zondervan PE, Weimar W, Balk AH (2002) Sequential monitoring of intragraft cytokine mRNA expression in relation to diastolic lef ventricular wall thickness and function early after heart transplantation. Clin Transplant 16:433–441CrossRefPubMedGoogle Scholar
  29. Douard H, Parrens E, Billes MA, Labbe L, Baudet E, Broustet JP (1997) Predictive factors of maximal aerobic capacity after cardiac transplantation. Eur Heart J 18:1823–1828PubMedGoogle Scholar
  30. Drexler H, Riede U, Münzel T, König H, Funke E, Just H (1992) Alterations of skeletal muscle in chronic heart failure. Circulation 85:1751–1759PubMedGoogle Scholar
  31. Egan JJ, Kalra S, Yonan N, Hasleton PS, Brooks N, Woodcock AA (1993) Pulmonary diffusion abnormalities in heart transplant recipients. Relationship to cytomegalovirus infection. Chest 104:1085–1089PubMedGoogle Scholar
  32. Ehrman J, Keteyian S, Fedel F, Rhoads K, Levine TB, Shepard R (1992) Cardiovascular responses of heart transplant recipients to graded exercise testing. J Appl Physiol 73:260–264PubMedGoogle Scholar
  33. Ewert R, Wensel R, Bruch L, Mutze S, Bauer U, Plauth M, Kleber FX (2000) Relationship between impaired pulmonary diffusion and cardiopulmonary exercise capacity after heart transplantation. Chest 117:968–975CrossRefPubMedGoogle Scholar
  34. Felici F, Turchetta A, Parisi F, Calzolari A, Marcelletti C (1996) Children's exercise capability after orthotopic heart transplant. Int J Sports Cardiol 5:61–66Google Scholar
  35. Ferretti G, Marconi C, Achilli G, Caspani E, Fiocchi R, Mamprin F, Gamba A, Ferrazzi P, Cerretelli P (2002) The heart rate response to exercise and circulating catecholamines in heart transplant recipients. Pflugers Archiv 443:370–376CrossRefPubMedGoogle Scholar
  36. Frist WH, Groves JR, Merrill WH, Connors AW, Stewart KA, Luce PA, Walker BL, Heim CR (1992) Physiological exercise responses in heart transplant recipients. Transplant Proc 24:2672–2673PubMedGoogle Scholar
  37. Geny B, Saini J, Mettauer B, Lampert E, Piquard F, Follenius M, Epailly E, Schnedecker B, Eisenmann B, Haberey P, Lonsdorfer J (1996) Effect of short-term endurance training on exercise capacity, haemodynamics and atrial natriuretic peptide secretion in heart transplant recipients. Eur J Appl Physiol 73:259–266Google Scholar
  38. Geny B, Charloux A, Lampert E, Londsdorfer J, Haberey P, Piquard F (1998) Enhanced brain natriuretic peptide response to peak exercise in heart transplant recipients. J Appl Physiol 85:2270–2276PubMedGoogle Scholar
  39. Givertz MM, Hartley LH, Colucci WS (1997) Long-term sequential changes in exercise capacity and chronotropic responsiveness after cardiac transplantation. Circulation 96:232–237PubMedGoogle Scholar
  40. Grassi B, Marconi C, Meyer M, Rieu M, Cerretelli P (1997) Gas exchange and cardiovascular kinetics with different exercise protocols in heart transplant recipients. J Appl Physiol 82:1952–1962PubMedGoogle Scholar
  41. Groen HJ, Bogaard JM, Balk AH, Kho SG, Hop WC, Hilvering C (1992) Diffusion capacity in heart transplant recipients. Chest 102:456–460PubMedGoogle Scholar
  42. Gullestad L, Haywood G, Ross H, Bjornerheim R, Geiran O, Kjekshus J, Simonsen S, Fowler M (1996) Exercise capacity of heart transplant recipients: the importance of chronotropic incompetence. J Heart Lung Transplant 15:1075–1083PubMedGoogle Scholar
  43. Hainsey T, Csiszar A, Sun S, Edwards JG (2002) Cyclosporin A does not block exercise-induced cardiac hypertrophy. Med Sci Sports Exerc 34:1249–1254PubMedGoogle Scholar
  44. Hall MJ, Snell GI, Side EA, Esmore DS, Walters EH, Williams TJ (1994) Exercise, potassium, and muscle deconditioning post-thoracic organ transplantation. J Appl Physiol 77:2784–2790PubMedGoogle Scholar
  45. Hertz MI, Taylor DO, Trulock EP, Boucek MM, Mohacsi PJ, Edwards LB, Keck BM (2002) The Registry of the International Society of Heart and Lung Transplantation: nineteenth official report—2002. J Heart Lung Transplant 21:950–970CrossRefPubMedGoogle Scholar
  46. Holm T, Aukrust P, Andreassen A, Brosstad F, Frøland SS, Simonsen S, Gullestad L (2000) Peripheral endothelial dysfunction in heart transplant recipients: possible role of proinflammatory cytokines. Clin Transplant 14:218–225CrossRefPubMedGoogle Scholar
  47. Hosenpud JD, Morton MJ, Wilson RA, Pantely GA, Norman DJ, Cobanoglu MA, Starr A (1989) Abnormal exercise hemodynamics in cardiac allograft recipients 1 year after cardiac transplantation. Relation to preload reserve Circulation 80:525–532Google Scholar
  48. Hosenpud JD, Stibolt TA, Atwal K, Shelley D (1990) Abnormal pulmonary function specifically related to congestive heart failure: comparison of patients before and after cardiac transplantation. Am J Med 88:493–496PubMedGoogle Scholar
  49. Hosenpud JD, Novick RJ, Breen TJ, Kedem J, Daily P (1995) The registry of the international society for heart and lung transplantation: 12th official report: 1995. J Heart Lung Transplant 14:805–815PubMedGoogle Scholar
  50. Hsu DT, Garofano RP, Douglas JM, Michler RE, Quaegebeur JM, Gersony WM, Addonizio LJ (1993) Exercise performance after pediatric heart transplantation. Circulation 88(2):238–242Google Scholar
  51. Jahnke AW, Leyh R, Guha M, Sievers HH, Bernhard A (1994) Time course of lung function and exercise performance after heart transplantation. J Heart Lung Transplant 13:412–417PubMedGoogle Scholar
  52. Jensen RL, Yanowitz FG, Crapo RO (1991) Exercise hemodynamics and oxygen delivery measurements using rebreathing techniques in heart transplant patients. Am J Cardiol 68:129–133PubMedGoogle Scholar
  53. Kao AC, Van Trigt P III, Shaeffer-McCall GS, Shaw JP, Kuzil BB, Page RD, Higginbotham MB (1994) Central and peripheral limitations to upright exercise in untrained cardiac transplant recipients. Circulation 89:2605–2615PubMedGoogle Scholar
  54. Kao AC, Van Trigt P III, Shaeffer-McCall GS, Shaw JP, Kuzil BB, Page RD, Higginbotham MB (1995) Allograft diastolic dysfunction and chronotropic incompetence limit cardiac output response to exercise two to six years after heart transplantation. J. Heart Lung Transplant 14:11–22Google Scholar
  55. Kavanagh T, Yacoub M, Campbell RB, Mertens DJ (1986) Marathon running after cardiac transplantation: a case history. J Cardiopulm Rehabil 6:16–20Google Scholar
  56. Kavanagh T, Yacoub MH, Mertens DJ, Kennedy J, Campbell RB, Sawyer P (1988) Cardiorespiratory responses to exercise training after orthotopic cardiac transplantation. Circulation 77:162–171PubMedGoogle Scholar
  57. Kemp DL, Jennison SH, Stelken AM, Younis LT, Miller LW (1995) Association of resting heart rate and chronotropic response. Am J Cardiol 75:751–752CrossRefPubMedGoogle Scholar
  58. Keteyian S, Shepard R, Ehrman J, Fedel F, Glick C, Rhoads K, Levine TB (1991) Cardiovascular responses of heart transplant patients to exercise training. J Appl Physiol 70:2627–2631PubMedGoogle Scholar
  59. Keteyian S, Marks CRC, Levine AB, Fedel F, Ehrman J, Kataoka T, Levine TB (1994) Cardiovascular responses of cardiac transplant patients to arm and leg exercise. Eur J Appl Physiol 68:441–444Google Scholar
  60. Kevelaitis E, Nyborg NC, Menasché P (1999) Coronary endothelial dysfunction of isolated hearts subjected to prolonged cold storage: patters and contributing factors. J Heart Lung Transplant 18:239–247CrossRefPubMedGoogle Scholar
  61. Labovitz AJ, Drimmer AM, McBride LR, Pennington DG, Willman VL, Miller LW (1989) Exercise capacity during the first year after cardiac transplantation. Am J Cardiol 64:642–645PubMedGoogle Scholar
  62. Lampert E, Mettauer B, Hoppeler H, Charloux A, Charpentier A, Lonsdorfer J (1996) Structure of skeletal muscle in heart transplant recipients. J Am Coll Cardiol 28:980–984PubMedGoogle Scholar
  63. Lampert E, Mettauer B, Hoppeler H, Charloux A, Charpentier A, Lonsdorfer J (1998) Skeletal muscle response to short endurance training in heart transplant recipients. J Am Coll Cardiol 32:420–426Google Scholar
  64. Lord SW, Brady S, Holt ND, Mitchell L, Dark JH, McComb JM (1996) Exercise response after cardiac transplantation: correlation with sympathetic reinnervation. Heart 75:40–43PubMedGoogle Scholar
  65. Lucini D, Milani RV, Ventura HO, Mehra MR, Messerli F, Pagani M (2000) Study of arterial and autonomic effects of cyclosporin in humans. Hypertension 35:1258–1263PubMedGoogle Scholar
  66. Mancini DM, Walter G, Reichek N, Lenkinski R, McCully KK, Mullen JL, Wilson JR (1992) Contribution of skeletal muscle atrophy to exercise intolerance and altered muscle metabolism in heart failure. Circulation 85:1364–1373PubMedGoogle Scholar
  67. Mandak JS, Aaronson KD, Mancini DM (1995) Serial assessment of exercise capacity after heart transplantation. J Heart Lung Transplant 14:468–478PubMedGoogle Scholar
  68. Marconi C, Grassi B, Meyer M, Cabrol A, Cerretelli P (1991) Ventilatory and gas exchange kinetics in a human recipient of a Jarvik-7 total artificial heart. J Appl Physiol 70:1406–1407PubMedGoogle Scholar
  69. Marconi C, Marzorati M, Fiocchi R, Mamprin F, Ferrazzi P, Ferretti G, Cerretelli P (2002) Age-related heart rate response to exercise in heart transplant recipients. Functional significance. Pflugers Archiv 443:698–706CrossRefPubMedGoogle Scholar
  70. Marzo KP, Wilson JR, Mancini DM (1992). Effects of cardiac transplantation on ventilatory response to exercise. Am J Cardiol 69:547–553PubMedGoogle Scholar
  71. Massie BM, Conway M, Rajagopalan B, Yonge R, Frostick S, Ledingham J, Sleight P, Radda G (1988) Skeletal muscle metabolism during exercise under ischemic conditions in congestive heart failure: evidence for abnormalities unrelated to blood flow. Circulation 78:320–326PubMedGoogle Scholar
  72. M'Bouh S, Bellmont S, Lampert E, Epailly E, Zoll J, N'Guessan B, Ribera F, Geny B, Oyono S, Arnold P, Lonsdorfer J, Mettauer B (2001) An impaired cardiodynamic phase contributes to the abnormalO2 kinetics at exercise onset in both congestive heart failure and heart transplant patients but results from differing mechanisms. Transplant Proc 33:3543–3545CrossRefPubMedGoogle Scholar
  73. Mettauer B, Lampert E, Petitjean P, Bogui P, Epailly E, Schnedecker B, Geny B, Eisenmann B, Haberey P, Lonsdorfer J (1996) Persistent exercise intolerance following cardiac transplantation despite normal oxygen transport. Int J Sports Med 17:277–286PubMedGoogle Scholar
  74. Mettauer B, Lampert E, Charloux A, Zhao QM, Epailly E, Oswald M, Frans A, Piquard F, Lonsdorfer J (1999) Lung membrane diffusing capacity, heart failure, and heart transplantation. Am J Cardiol 83:62–67CrossRefPubMedGoogle Scholar
  75. Mettauer B, Zhao QM, Epailly E, Charloux A, Lampert E, Heitz-Naegelen B, Piquard F, di Prampero PE, Lonsdorfer J (2000)O2 kinetics reveal a central limitation at the onset of subthreshold exercise in heart transplant recipients. J Appl Physiol 88:1228–1238PubMedGoogle Scholar
  76. Meyer M, Cerretelli P, Marconi C, Rieu M, Chabrol C (1989) Cardiorespiratory adjustment to exercise after cardiac transplantation. In: Reinhart K, Eyrich K (eds) Clinical aspects of O2 transport and tissue oxygenation, vol 49. Springer, Berlin Heidelberg New York, pp 477–499Google Scholar
  77. Morales P, Cremades MJ, Pallardò L, Pastor A, Macian V (1995) Effects of cyclosporine on lung diffusing capacity in renal transplant patients. Transpl Int 8:481–484PubMedGoogle Scholar
  78. Ngimbous BB, Bourgeois F, Mas C, Simonneau M, Maolic JM (2001) Heart transplantation changes the expression of distinct gene families. Physiol Genomics 7:115–126PubMedGoogle Scholar
  79. Niset G, Poortmans JR, Leclercq R, Brasseur M, Desmet JM, Degre S, Primo G (1985) Metabolic implications during a 20-km run after heart transplantation. Int J Sport Med 6:340–343Google Scholar
  80. Nixon PA, Fricker FJ, Noyes BE, Webber SA, Orenstein DM, Armitage JM (1995) Exercise testing in pediatric heart, heart–lung, and lung transplant recipients. Chest 107:1328–1335PubMedGoogle Scholar
  81. Notarius, CF, Levy RD, Tully A, Fitchett D, Magder S (1998) Cardiac versus noncardiac limits to exercise after heart transplantation. Am Heart J 135:339–348PubMedGoogle Scholar
  82. Ohar J, Osterloh J, Ahmed N, Miller L (1993) Diffusing capacity decreases after transplantation. Chest 103:857–861PubMedGoogle Scholar
  83. Osada N, Chaitman BR, Donohue TJ, Wolford TL, Stelken AM, Miller LW (1997) Long-term cardiopulmonary exercise performance after heart transplantation. Am J Cardiol 79:451–456CrossRefPubMedGoogle Scholar
  84. Owen VJ, Burton PBJ, Michel MC, Zolk O, Bohm M, Pepper JR, Barton PJR, Yacoub MH, Harding SE (1999) Myocardial dysfunction in donor hearts. A possible etiology. Circulation 99:2565–2570PubMedGoogle Scholar
  85. Paterson DH, Cunningham DA, Pickering JG, Babcock MA, Boughner DR (1994) Oxygen uptake kinetics in cardiac transplant recipients. J Appl Physiol 77:1935–1940PubMedGoogle Scholar
  86. Paulus WJ, Bronzwaer JGF, Felice H, Kishan N, Wellens F (1992) Deficient acceleration of left ventricular relaxation during exercise after heart transplantation. Circulation 86:1175–1185PubMedGoogle Scholar
  87. Perez O, Castro P, Diaz-Araya G, Nettle D, Moraga F, Chiong M, Jalil J, Zalaquett R, Moran S, Becker P, Corbalan R, Lavandere S (2002) Persistence of oxidative stress after heart transplantation: a comparative study of patients with heart transplant versus chronic stable heart failure. Rev Esp Cardiol 55:831–837PubMedGoogle Scholar
  88. Perrault H, Melin B, Jimenez C, Dureau G, Allevard AM, Cottet-Emard JM, Gauquelin G, Gharib C (1994) Fluid-regulation and sympathoadrenal hormonal responses to peak exercise following cardiac transplantation. J Appl Physiol 76:230–235PubMedGoogle Scholar
  89. Piquard F, Charloux A, Mettauer B, Epailly E, Lonsdorfer E, Popescu S, Lonsdorfer J, Geny B (2000) Exercise-induced increase in circulating adrenomedullin is related to mean blood pressure in heart transplant recipients. J Clin Endocrinol Metab 85:2828–2831Google Scholar
  90. Preumont N, Berkenboom G, Vachiery JL, Jansens J-L, Antoine M, Wikler D, Damhaut P, Degré S, Lenaers A, Goldman S (2000) Early alterations in myocardial blood flow reserve in heart transplant recipients with angiographically normal coronary arteries. J Heart Lung Transplant 19:538–545CrossRefPubMedGoogle Scholar
  91. Quaini F, Urbanek K, Beltrami AP, Finato N, Beltrami CA, Nadal-Ginard B, Kaistura J, Leri A, Anversa P (2002) Chimerism of the transplanted heart. N Engl J Med 346:5–15PubMedGoogle Scholar
  92. Quigg R, Rocco MB, Gauthier DF, Creager MA, Hartley LH, Colucci WS (1989) Mechanism of the attenuated peak heart rate response to exercise after orthotopic cardiac transplantation. J Am Coll Cardiol 14:338–344Google Scholar
  93. Quigg R, Salyer J, Mohanty PK, Simpson P (1998) Impaired exercise capacity late after cardiac transplantation: influence of chronotropic incompetence, hypertension, and calcium channel blockers. Am Heart J 136:465–473PubMedGoogle Scholar
  94. Renlund DG, Taylor DO, Ensley RD, O'Connell JB, Gilbert EM, Bristow MR, Ma H, Yanowitz FG (1996) Exercise capacity after heart transplantation: influence of donor and recipient characteristics. J Heart Lung Transplant 15:16–24PubMedGoogle Scholar
  95. Richard R, Verdier JC, Duvallet A, Rosier S-P, Leger P, Nignan A, Rieu M (1999) Chronotropic competence in endurance trained heart transplant recipients: heart rate is not a limiting factor for exercise capacity. J Am Coll Cardiol 33:192–197Google Scholar
  96. Rowell LB, O'Leary DS (1990) Reflex control of the circulation during exercise: chemoreflexes and mechanoreflexes. J Appl Physol 69:407–418Google Scholar
  97. Rudas L, Pflugfelder PW, McKenzie FN, Menkis AH, Novick RJ, Kostuk WJ (1992) Normalization of upright exercise hemodynamics and improved exercise capacity one year after orthotopic cardiac transplantation. Am J Cardiol 69:1336–1339PubMedGoogle Scholar
  98. Savin WM, Alderman EL, Haskell WL, Schroeder JS, Ingels NB Jr, Daughters GT II, Stinson EB (1980) Left ventricular response to isometric exercise in patients with denervated and innervated hearts. Circulation 61:897–901PubMedGoogle Scholar
  99. Schaufelberger M, Eriksson BO, Lönn L, Rundqvist B, Stibrant Sunnerhagen K, Swedberg K (2001) Skeletal muscle characteristics, muscle strength and thigh muscle area in patients before and after cardiac transplantation. Eur J Heart Fail 3:59–67CrossRefGoogle Scholar
  100. Scherrer U, Vissing SF, Morgan, BJ, Rollins JA, Tindall RS, Ring S, Hanson P, Mohanty, PK, Victor RG (1990) Cyclosporin-induced sympathetic activation and hypertension after heart transplantation. N Engl J Med 323:693–699PubMedGoogle Scholar
  101. Schimke I, Schikora M, Meyer R, Dubel HP, Modersohn D, Kleber FX, Baumann G (2000) Oxidative stress in the human heart is associated with changes in the antioxidative defence as shown after heart transplantation. Mol Cell Biochem 204:89–96CrossRefPubMedGoogle Scholar
  102. Schmidt A, Pleiner J, Bayerle-Eder M, Wiesinger GF, Rödler S, Quittan M, Mayer G, Woltz M (2002) Regular physical exercise improves endothelial function in heart transplant recipients. Clin Transplant 16:137–143CrossRefPubMedGoogle Scholar
  103. Schwaiblmair M, von Scheidt W, Überfuhr P, Ziegler S, Schwaiger M, Reichart B, Vogelmeier C (1999a) Functional significance of cardiac reinnervation in heart transplant recipients. J Heart Lung Transplant 18:838–845CrossRefPubMedGoogle Scholar
  104. Schwaiblmair M, von Scheidt W, Überfuhr P, Reichart B, Vogelmeier C (1999b) Lung function and cardiopulmonary exercise performance after heart transplantation: influence of cardiac allograft vasculopathy. Chest 116:332–339CrossRefPubMedGoogle Scholar
  105. Schwaiger M, Hutchins GD, Kalff V, Rosenspire K, Haka MS, Mallette S, Deeb GM, Abrams GD, Wieland D (1991) Evidence for regional catecholamine uptake and storage sites in the transplanted human heart by positron emission tomography. J Clin Invest 87:1681–1690PubMedGoogle Scholar
  106. Squires RW (1991) Exercise training after cardiac transplantation. Med Sci Sports Exerc 23:686–694PubMedGoogle Scholar
  107. Stevenson LW, Sietsema K, Tillisch JH, Lem V, Walden J, Kobashigawa JA, Moriguchi J (1990) Exercise capacity for survivors of cardiac transplantation or sustained medical therapy for stable heart failure. Circulation 81:78–85PubMedGoogle Scholar
  108. Stratton JR, Kemp GJ, Daly RC, Yacoub M, Rajagopalan B (1994) Effects of cardiac transplantation on bioenergetic abnormalities of skeletal muscle in congestive heart failure. Circulation 89:1624–1631PubMedGoogle Scholar
  109. Sullivan MJ, Higginbotham MB, Cobb FR (1988) Increased exercise ventilation in patients with chronic heart failure: intact ventilatory control despite hemodynamic and pulmonary abnormalities. Circulation 77:552–559PubMedGoogle Scholar
  110. Toledo E, Pinhas I, Aravot D, Almog Y, Akselrod S (2002) Functional restitution of cardiac control in heart transplant patients Am J Physiol 282:R900–R908Google Scholar
  111. Uretsky BF, Murali S, Reddy PS, Rabin B, Lee A, Griffith BP, Hardesty RL, Trento A, Bahnson HT (1987) Development of coronary artery disease in cardiac transplant patients receiving immunosuppressive therapy with cyclosporin and prednisone. Circulation 76:827–834PubMedGoogle Scholar
  112. Ville N, Mercier J, Varray A, Albat B, Messner-Pellenc P, Préfaut C (1998) Exercise tolerance in heart transplant patients with altered pulmonary diffusion capacity. Med Sci Sports Exerc 30:339–344PubMedGoogle Scholar
  113. Wiener DH, Fink LI, Maris J, Jones RA, Chance B, Wilson JR (1986) Abnormal skeletal muscle bioenergetics during exercise in patients with heart failure: role of reduced muscle blood flow. Circulation 73:1127–1136PubMedGoogle Scholar
  114. Wilson RF, Johnson TH, Haidet GC, Kubo SH, Mianuelli M (2000) Sympathetic reinnervation of the sinus node and exercise hemodynamics after cardiac transplantation. Circulation 101:2727–2733PubMedGoogle Scholar
  115. Wright RS, Levine MS, Bellamy PE, Simmons MS, Batra P, Stevenson LW, Walden JA, Laks H, Tashkin DP (1990) Ventilatory and diffusion abnormalities in potential heart transplant recipients. Chest 98:816–820PubMedGoogle Scholar
  116. Zhao QM, Mettauer B, Epailly E, Falkenrodt A, Lampert E, Charloux A, Charpentier A, Lonsdorfer J (1998) Effect of exercise training on leukocyte subpopulations and clinical course in cardiac transplant patients Transplant Proc 30:172–175CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Muscle Physiology and Proteome Section I.B.F.M.-Consiglio Nazionale delle Ricerche, L.I.T.A.MilanItaly

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