Exercise after Heart Transplantation: Typical Alterations,
                    Diagnostics and Interventions

Thomas Schmidt; Birna Bjarnason-Wehrens; Hans-Georg Predel; Nils Reiss

doi:10.1055/a-1194-4995

International Journal of Sports Medicine, Inhaltsverzeichnis

Int J Sports Med 2021; 42(02): 103-111
DOI: 10.1055/a-1194-4995

Review

Exercise after Heart Transplantation: Typical Alterations, Diagnostics and Interventions

Thomas Schmidt

¹Institute for Cardiovascular Research, Schüchtermann-Klinik Bad Rothenfelde, Bad Rothenfelde, Germany

²Department of Preventive and Rehabilitative Sport and Exercise Medicine, Institute for Cardiology and Sports Medicine, Cologne, German Sport University Cologne, Germany

,

Birna Bjarnason-Wehrens

²Department of Preventive and Rehabilitative Sport and Exercise Medicine, Institute for Cardiology and Sports Medicine, Cologne, German Sport University Cologne, Germany

,

Hans-Georg Predel

²Department of Preventive and Rehabilitative Sport and Exercise Medicine, Institute for Cardiology and Sports Medicine, Cologne, German Sport University Cologne, Germany

,

Nils Reiss

¹Institute for Cardiovascular Research, Schüchtermann-Klinik Bad Rothenfelde, Bad Rothenfelde, Germany

› Institutsangaben

Abstract

For the treatment of terminal heart failure, heart transplantation is considered to be the gold standard, leading to significantly improved quality of life and long-time survival. For heart transplant recipients, the development and maintenance of good functional performance and adequate exercise capacity is crucial for renewed participation and integration in self-determined live. In this respect, typical transplant-related alterations must be noted that play a significant role, leading to restrictions both centrally and peripherally. Before patients begin intensive and structured exercise training, a comprehensive diagnosis of their exercise capacity should take place in order to stratify the risks involved and to plan the training units accordingly. Particularly endurance sports and resistance exercises are recommended to counter the effects of the underlying disease and the immunosuppressive medication. The performance level achieved can vary considerably depending on their individual condition, from gentle activity through a non-competitive-level to intensive competitive sports. This paper includes an overview of the current literature on heart transplant recipients, their specific characteristics, as well as typical cardiovascular and musculoskeletal alterations. It also discusses suitable tools for measuring exercise capacity, recommendations for exercise training, required precautions and the performance level usually achieved.

Key words

heart failure - heart transplantation - transplant-related alterations - exercise testing - exercise training - exercise capacity

Volltext

Referenzen

References
1 Yancy CW, Jessup M, Bozkurt B. et al. 2013 ACCF/AHA guideline for the management of heart failure: A report of the American College of Cardiology Foundation/American Heart Association Task Force on Practice Guidelines. J Am Coll Cardiol 2013; 62: e147-e239
2 Mosterd A, Hoes AW. Clinical epidemiology of heart failure. Heart 2007; 93: 1137-1146
3 Roger VL, Weston SA, Redfield MM. et al. Trends in heart failure incidence and survival in a community-based population. JAMA 2004; 292: 344-350
4 Stehlik J, Kobashigawa J, Hunt SA. et al. Honoring 50 years of clinical heart transplantation in circulation: in-depth state-of-the-art review. Circulation 2018; 137: 71-87
5 Emin A, Rogers CA, Banner NR. Quality of life of advanced chronic heart failure: Medical care, mechanical circulatory support and transplantation. Eur J Cardiothorac Surg 2016; 50: 269-273
6 Lund LH, Edwards LB, Kucheryavaya AY. et al. The Registry of the International Society for Heart and Lung Transplantation: Thirty-second Official Adult Heart Transplantation Report – 2015; Focus Theme: Early Graft Failure. J Heart Lung Transplant 2015; 34: 1244-1254
7 Khush KK, Cherikh WS, Chambers DC. et al. The International Thoracic Organ Transplant Registry of the International Society for Heart and Lung Transplantation: Thirty-sixth adult heart transplantation report – 2019; Focus theme: Donor and Recipient Size Match. J Heart Lung Transplant 2019; 38: 1056-1066
8 Lund LH, Edwards LB, Dipchand AI. et al. The Registry of the International Society for Heart and Lung Transplantation: Thirty-third Adult Heart Transplantation Report– 2016; Focus Theme: Primary Diagnostic Indications for Transplant. J Heart Lung Transplant 2016; 35: 1158-1169
9 Lund LH, Khush KK, Cherikh WS. et al. The Registry of the International Society for Heart and Lung Transplantation: Thirty-fourth Adult Heart Transplantation Report – 2017; Focus Theme: Allograft Ischemic Time. J Heart Lung Transplant 2017; 36: 1037-1046
10 Brown CR, Khurshan F, Chen Z. et al. Optimal timing for heart transplantation in patients bridged with left ventricular assist devices: Is timing of the essence?. J Thorac Cardiovasc Surg 2019; 157: 2315.e4-2324.e4
11 Shiner CT, Woodbridge G, Skalicky DA. et al. Multidisciplinary inpatient rehabilitation following heart and/or lung transplantation – examining cohort characteristics and clinical outcomes. PM R 2019; 11: 849-857
12 Bjarnason-Wehrens B, Schmidt T, Reiss N. Exercise in specific diseases: heart transplantation and left ventricular assist device. In: Pressler A, Niebauer J, Eds. Textbook of Sports and Exercise Cardiology : Springer International Publishing; 2020: 977-1009
13 Kavanagh T, Mertens DJ, Shephard RJ. et al. Long-term cardiorespiratory results of exercise training following cardiac transplantation. Am J Cardiol 2003; 91: 190-194
14 Zoll J, N’Guessan B, Ribera F. et al. Preserved response of mitochondrial function to short-term endurance training in skeletal muscle of heart transplant recipients. J Am Coll Cardiol 2003; 42: 126-132
15 Braith RW, Magyari PM, Pierce GL. et al. Effect of resistance exercise on skeletal muscle myopathy in heart transplant recipients. Am J Cardiol 2005; 95: 1192-1198
16 Bussières LM, Pflugfelder PW, Taylor AW. et al. Changes in skeletal muscle morphology and biochemistry after cardiac transplantation. Am J Cardiol 1997; 79: 630-634
17 Stratton JR, Kemp GJ, Daly RC. et al. Effects of cardiac transplantation on bioenergetic abnormalities of skeletal muscle in congestive heart failure. Circulation 1994; 89: 1624-1631
18 Lampert E, Mettauer B, Hoppeler H. et al. Structure of skeletal muscle in heart transplant recipients. J Am Coll Cardiol 1996; 28: 980-984
19 Braith RW, Edwards DG. Exercise following heart transplantation. Sports Med 2000; 30: 171-192
20 Henderson NK, Sambrook PN, Kelly PJ. et al. Bone mineral loss and recovery after cardiac transplantation. Lancet 1995; 346: 905
21 Kobashigawa J, Olymbios M. Physiology of the transplanted heart. In: Kobashigawa J, Ed. Clinical Guide to Heart Transplantation Springer International Publishing; 2017: 81-93
22 Awad M, Czer LSC, Hou M. et al. Early Denervation and later reinnervation of the heart following cardiac transplantation: A review. J Am Heart Assoc 2016; 5: e004070
23 Kim IC, Youn JC, Kobashigawa JA. The Past, Present and Future of Heart Transplantation. Korean Circ J 2018; 48: 565-590
24 Tallaj JA, Kirklin JK, Brown RN. et al. Post-heart transplant diastolic dysfunction is a risk factor for mortality. J Am Coll Cardiol 2007; 50: 1064-1069
25 Paulus WJ, Bronzwaer JG, Felice H. et al. Deficient acceleration of left ventricular relaxation during exercise after heart transplantation. Circulation 1992; 86: 1175-1185
26 Kao AC, van Trigt P, Shaeffer-McCall GS. et al. Central and peripheral limitations to upright exercise in untrained cardiac transplant recipients. Circulation 1994; 89: 2605-2615
27 Pflugfelder PW, Purves PD, McKenzie FN. et al. Cardiac dynamics during supine exercise in cyclosporine-treated orthotopic heart transplant recipients: Assessment by radionuclide angiography. J Am Coll Cardiol 1987; 10: 336-341
28 Braith RW, Clapp L, Brown T. et al. Rate-responsive pacing improves exercise tolerance in heart transplant recipients: A pilot study. J Cardiopulm Rehabil 2000; 20: 377-382
29 Braith RW, Wood CE, Limacher MC. et al. Abnormal neuroendocrine responses during exercise in heart transplant recipients. Circulation 1992; 86: 1453-1463
30 Costanzo MR, Dipchand A, Starling R. et al. The International Society of Heart and Lung Transplantation Guidelines for the care of heart transplant recipients. J Heart Lung Transplant 2010; 29: 914-956
31 Squires RW. Exercise therapy for cardiac transplant recipients. Prog Cardiovasc Dis 2011; 53: 429-436
32 Vanhees L, Rauch B, Piepoli M. et al. Importance of characteristics and modalities of physical activity and exercise in the management of cardiovascular health in individuals with cardiovascular disease (Part III). Eur J Prev Cardiol 2012; 19: 1333-1356
33 Rosenbaum AN, Kremers WK, Schirger JA. et al. Association between early cardiac rehabilitation and long-term survival in cardiac transplant recipients. Mayo Clin Proc 2016; 91: 149-156
34 Anderson L, Nguyen TT, Dall CH. et al. Exercise-based cardiac rehabilitation in heart transplant recipients. Cochrane Database Syst Rev 2017; 4: CD012264
35 Nytrøen K, Gullestad L. Exercise after heart transplantation: an overview. World J Transplant 2013; 3: 78-90
36 Hsieh P-L, Wu Y-T, Chao W-J. Effects of exercise training in heart transplant recipients: a meta-analysis. Cardiology 2011; 120: 27-35
37 Didsbury M, McGee RG, Tong A. et al. Exercise training in solid organ transplant recipients: a systematic review and meta-analysis. Transplantation 2013; 95: 679-687
38 Tegtbur U, Busse MW, Jung K. et al. Time course of physical reconditioning during exercise rehabilitation late after heart transplantation. J Heart Lung Transplant 2005; 24: 270-274
39 Pascoalino LN, Ciolac EG, Tavares AC. et al. Exercise training improves ambulatory blood pressure but not arterial stiffness in heart transplant recipients. J Heart Lung Transplant 2015; 34: 693-700
40 Schmidt A, Pleiner J, Bayerle-Eder M. et al. Regular physical exercise improves endothelial function in heart transplant recipients. Clin Transplant 2002; 16: 137-143
41 Braith RW, Schofield RS, Hill JA. et al. Exercise training attenuates progressive decline in brachial artery reactivity in heart transplant recipients. J Heart Lung Transplant 2008; 27: 52-59
42 Pierce GL, Schofield RS, Casey DP. et al. Effects of exercise training on forearm and calf vasodilation and proinflammatory markers in recent heart transplant recipients: A pilot study. Eur J Cardiovas Prev Rehabil 2008; 15: 10-18
43 Karapolat H, Engin C, Eroglu M. et al. Efficacy of the cardiac rehabilitation program in patients with end-stage heart failure, heart transplant patients, and left ventricular assist device recipients. Transplant Proc 2013; 45: 3381-3385
44 Tegtbur U, Busse MW, Jung K. et al. Phase III rehabilitation after heart transplantation. Z Kardiol 2003; 92: 908-915
45 Wu Y-T, Chien C-L, Chou N-K. et al. Efficacy of a home-based exercise program for orthotopic heart transplant recipients. Cardiology 2008; 111: 87-93
46 Kugler C, Malehsa D, Tegtbur U. et al. Health-related quality of life and exercise tolerance in recipients of heart transplants and left ventricular assist devices: A prospective, comparative study. J Heart Lung Transplant 2011; 30: 204-210
47 Nytrøen K, Rolid K, Andreassen AK. et al. Effect of high-intensity interval training in de novo heart transplant recipients in Scandinavia. Circulation 2019; 139: 2198-2211
48 Nytrøen K, Rustad LA, Aukrust P. et al. High-intensity interval training improves peak oxygen uptake and muscular exercise capacity in heart transplant recipients. Am J Transplant 2012; 12: 3134-3142
49 Rustad LA, Nytrøen K, Amundsen BH. et al. One year of high-intensity interval training improves exercise capacity, but not left ventricular function in stable heart transplant recipients: a randomised controlled trial. Eur J Prev Cardiol 2014; 21: 181-191
50 Monk-Hansen T, Dall CH, Christensen SB. et al. Interval training does not modulate diastolic function in heart transplant recipients. Scand Cardiovasc J 2014; 48: 91-98
51 Nytrøen K, Rustad LA, Erikstad I. et al. Effect of high-intensity interval training on progression of cardiac allograft vasculopathy. J Heart Lung Transplant 2013; 32: 1073-1080
52 Hermann TS, Dall CH, Christensen SB. et al. Effect of high intensity exercise on peak oxygen uptake and endothelial function in long-term heart transplant recipients. Am J Transplant 2011; 11: 536-541
53 Christensen SB, Dall CH, Prescott E. et al. A high-intensity exercise program improves exercise capacity, self-perceived health, anxiety and depression in heart transplant recipients: A randomized, controlled trial. J Heart Lung Transplant 2012; 31: 106-107
54 Dall CH, Snoer M, Christensen S. et al. Effect of high-intensity training versus moderate training on peak oxygen uptake and chronotropic response in heart transplant recipients: a randomized crossover trial. Am J Transplant 2014; 14: 2391-2399
55 Dall CH, Gustafsson F, Christensen SB. et al. Effect of moderate- versus high-intensity exercise on vascular function, biomarkers and quality of life in heart transplant recipients: A randomized, crossover trial. J Heart Lung Transplant 2015; 34: 1033-1041
56 Conraads VM, Pattyn N, Maeyer Cde. et al. Aerobic interval training and continuous training equally improve aerobic exercise capacity in patients with coronary artery disease: The SAINTEX-CAD study. Int J Cardiol 2015; 179: 203-210
57 Ellingsen Ø, Halle M, Conraads V. et al. High-intensity interval training in patients with heart failure with reduced ejection fraction. Circulation 2017; 135: 839-849
58 Taylor JL, Holland DJ, Spathis JG. et al. Guidelines for the delivery and monitoring of high intensity interval training in clinical populations. Prog Cardiovasc Dis 2019; 62: 140-146
59 Braith RW, Mills RM, Welsch MA. et al. Resistance exercise training restores bone mineral density in heart transplant recipients. J Am Coll Cardiol 1996; 28: 1471-1477
60 Braith RW, Welsch MA, Mills RM. et al. Resistance exercise prevents glucocorticoid-induced myopathy in heart transplant recipients. Med Sci Sports Exerc 1998; 30: 483-489
61 Braith RW, Magyari PM, Fulton MN. et al. Resistance exercise training and alendronate reverse glucocorticoid-induced osteoporosis in heart transplant recipients. J Heart Lung Transplant 2003; 22: 1082-1090
62 Dew MA, Kormos RL, DiMartini AF. et al. Prevalence and risk of depression and anxiety-related disorders during the first three years after heart transplantation. Psychosomatics 2001; 42: 300-313
63 DeCampli WM. Of mice and men … does exercise decrease progression of transplant coronary vasculopathy?. J Thorac Cardiovasc Surg 2015; 149: 337-339
64 Crespo-Leiro MG, Metra M, Lund LH. et al. Advanced heart failure: a position statement of the Heart Failure Association of the European Society of Cardiology. Eur Heart J 2018; 20: 1505-1535
65 Malhotra R, Bakken K, D’Elia E. et al. Cardiopulmonary exercise testing in heart failure. JACC Heart Fail 2016; 4: 607-616
66 Mathur S, Janaudis-Ferreira T, Wickerson L. et al. Meeting report: consensus recommendations for a research agenda in exercise in solid organ transplantation. Am J Transplant 2014; 14: 2235-2245
67 Tsai H-Y, Tsai W-J, Kuo L-Y. et al. Oxygen consumption at anaerobic threshold predicts cardiac events after heart transplantation. Transplant Proc 2018; 50: 2742-2746
68 Yardley M, Havik OE, Grov I. et al. Peak oxygen uptake and self-reported physical health are strong predictors of long-term survival after heart transplantation. Clin Transplant 2016; 30: 161-169
69 Raichlin E, Selim A, Zolty R. et al. Cardiopulmonary stress test one year after HTx predicts the development of CAV. J Heart Lung Transplant 2017; 36: S296
70 Doutreleau S, Di Marco P, Talha S. et al. Can the six-minute walk test predict peak oxygen uptake in men with heart transplant?. Arch Phys Med Rehabil 2009; 90: 51-57
71 American Thoracic Society. ATS statement: guidelines for the six-minute walk test. Am J Respir Crit Care Med 2002; 166: 111-117
72 Podsiadlo D, Richardson S. The timed “Up & Go”: A test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 1991; 39: 142-148
73 Guazzi M, Arena R, Halle M. et al. 2016 focused update: Clinical recommendations for cardiopulmonary exercise testing data assessment in specific patient populations. Eur Heart J 2018; 39: 1144-1161
74 Reiss N, Schmidt T, Mommertz S. et al. Inert gas rebreathing – helpful tool in the management of left ventricular assist device patients. Perfusion 2018; 33: 335-338
75 Agostoni P, Cattadori G, Apostolo A. et al. Noninvasive measurement of cardiac output during exercise by inert gas rebreathing technique: a new tool for heart failure evaluation. J Am Coll Cardiol 2005; 46: 1779-1781
76 Innes E. Handgrip strength testing: A review of the literature. Aust Occup Ther J 1999; 46: 120-140
77 Reynolds JM, Gordon TJ, Robergs RA. Prediction of one repetition maximum strength from multiple repetition maximum testing and anthropometry. J Strength Cond Res 2006; 20: 584-592
78 Guazzi M, Bandera F, Ozemek C. et al. Cardiopulmonary exercise testing: What is its value?. J Am Coll Cardiol 2017; 70: 1618-1636
79 Pescatello LS. ed. ACSM’s Guidelines for Exercise Testing and Prescription. 9^th ed. Baltimore, MD/Philadelphia, PA: Wolters Kluwer Lippincott Williams & Wilkins; 2014
80 Berg K, Bjerre K, Clemmensen T. et al. Silent ischemia and arrhythmia after heart transplantation: relation to cardiac allograft vasculopathy. J Heart Lung Transplant 2019; 38: S282
81 Ehrman JK, Keteyian SJ, Levine AB. et al. Exercise stress tests after cardiac transplantation. Am J Cardiol 1993; 71: 1372-1373
82 Skorić B, Čikeš M, Ljubas Maček J. et al. Cardiac allograft vasculopathy: diagnosis, therapy, and prognosis. Croat Med J 2014; 55: 562-576
83 Gustafsson F, Hunt SA, Yeon SB. Heart transplantation: clinical manifestations, diagnosis, and prognosis of cardiac allograft vasculopathy. UpToDate. Retrieved May 15, 2020, from https://www.uptodate.com/contents/heart-transplantation-clinical-manifestations-diagnosis-and-prognosis-of-cardiac-allograft-vasculopathy
84 Sieg A, Weeks P, Krustchinsky L. et al. Statin therapy in cardiac allograft vasculopathy progression in heart transplant patients: Does potency matter?. Transplant Rev (Orlando) 2016; 30: 178-186
85 Vilchez RA, Fung J, Kusne S. Cryptococcosis in organ transplant recipients: an overview. Am J Transplant 2002; 2: 575-580
86 Cordes C. 4.10. Patienten nach Herztransplantation (HTX). In: AWMF - Arbeitsgemeinschaft der Wissenschaftlichen Medizinischen Fachgesellschaften, Ed. S3-Leitlinie zur kardiologischen Rehabilitation (LL-KardReha) im deutschsprachigen Raum Europas: Deutschland, Österreich, Schweiz (D-A-CH). Langversion – Teil 2020; 1: 91-94
87 Kelly RL, Walsh JR, Paratz JD. et al. Quadriceps muscle strength and body mass index are associated with estimates of physical activity postheart transplantation. Transplantation 2019; 103: 1253-1259
88 Chen S-Y, Lu P-C, Lan C. et al. Six-minute walk test among heart transplant recipients. Transplant Proc 2014; 46: 929-933
89 Anyanwu A, Treasure T. Prognosis after heart transplantation: Transplants alone cannot be the solution for end stage heart failure. BMJ 2003; 326: 509-510
90 Givertz MM, Hartley LH, Colucci WS. Long-term sequential changes in exercise capacity and chronotropic responsiveness after cardiac transplantation. Circulation 1997; 96: 232-237
91 Schmidt T, Bjarnason-Wehrens B, Bartsch P. et al. Exercise capacity and functional performance in heart failure patients supported by a left ventricular assist device at discharge from inpatient rehabilitation. Artif Organs 2018; 42: 22-30
92 Schmidt T, Bjarnason-Wehrens B, Mommertz S. et al. Development of exercise-related values in heart failure patients supported with a left ventricular assist device. Int J Artif Organs 2019; 42: 201-206
93 Haykowsky MJ, Halle M, Baggish A. Upper limits of aerobic power and performance in heart transplant recipients: Legacy effect of prior endurance training. Circulation 2018; 137: 650-652
94 Harriss DJ, MacSween A, Atkinson G. Ethical standards in sport and exercise science research: 2020 update. Int J Sports Med 2019; 40: 813-817