Defining cardiac adaptations and safety of endurance training in patients with m.3243A>G-related mitochondrial disease

International Journal of Cardiology

Volumn 168, Issue 4, 2013, Pages 3599-3608

  Bates, Matthew G D ^a,b   Newman, Jane H ^a   Jakovljevic, Djordje G ^a,c   Hollingsworth, Kieren G ^c   Alston, Charlotte L ^a   Zalewski, Pawel ^d   Klawe, Jacek J ^d   Blamire, Andrew M ^c   Macgowan, Guy A ^b,e   Keavney, Bernard D ^b,e   Bourke, John P ^b   Schaefer, Andrew ^a,c   McFarland, Robert ^a,c   Newton, Julia L ^c   Turnbull, Douglass M ^a,c   Taylor, Robert W ^a   Trenell, Michael I ^c   Gorman, Gráinne S ^a,c  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b FREEMAN HOSPITAL   (United Kingdom)

^c NEWCASTLE UNIVERSITY   (United Kingdom)

^d NICOLAUS COPERNICUS UNIVERSITY   (Poland)

^e NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Autonomic function; Cardiac magnetic resonance imaging; Cardiac magnetic resonance spectroscopy; Cardio pulmonary exercise testing; Endurance exercise; Mitochondrial DNA

Indexed keywords

ACCELEROMETER; ADULT; ANAEROBIC THRESHOLD; ARTICLE; BICYCLE ERGOMETER; BIOENERGY; BLOOD PRESSURE VARIABILITY; BODY PLETHYSMOGRAPHY; CARDIOVASCULAR MAGNETIC RESONANCE; CLINICAL ARTICLE; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENDURANCE TRAINING; EXERCISE TOLERANCE; FATIGUE; FEMALE; HEART FUNCTION; HEART LEFT VENTRICLE ENDDIASTOLIC VOLUME; HEART LEFT VENTRICLE MASS; HEART RATE VARIABILITY; HUMAN; MALE; OXYGEN CONSUMPTION; PHOSPHORUS NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; QUALITY OF LIFE; WORK CAPACITY;

AUTONOMIC FUNCTION; CARDIAC MAGNETIC RESONANCE IMAGING; CARDIAC MAGNETIC RESONANCE SPECTROSCOPY; CARDIO-PULMONARY EXERCISE TESTING; ENDURANCE EXERCISE; MITOCHONDRIAL DNA;

ADAPTATION, PHYSIOLOGICAL; ADULT; CARDIAC OUTPUT; COHORT STUDIES; EXERCISE TEST; EXERCISE TOLERANCE; FEMALE; FOLLOW-UP STUDIES; HUMANS; MALE; MIDDLE AGED; MITOCHONDRIAL DISEASES; PHYSICAL ENDURANCE; POINT MUTATION;

EID: 84886287512     PISSN: 01675273     EISSN: 18741754     Source Type: Journal    
DOI: 10.1016/j.ijcard.2013.05.062     Document Type: Article

References (71)

1. A.M. Schaefer, R. McFarland, and E.L. Blakely Prevalence of mitochondrial DNA disease in adults Ann Neurol 63 2008 35 39
2. H.R. Elliott, D.C. Samuels, J.A. Eden, C.L. Relton, and P.F. Chinnery Pathogenic mitochondrial DNA mutations are common in the general population Am J Hum Genet 83 2008 254 260
3. M.G.D. Bates, J.P. Bourke, C. Giordano, G. d'Amati, D.M. Turnbull, and R.W. Taylor Cardiac involvement in mitochondrial DNA disease: clinical spectrum, diagnosis, and management Eur Heart J 33 2012 3023 3033
4. G. Pfeffer, K. Majamaa, D.M. Turnbull, D. Thorburn, and P.F. Chinnery Treatment for mitochondrial disorders Cochrane Database Syst Rev 4 2012 [CD004426]
5. T. Taivassalo, N. De Stefano, and Z. Argov Effects of aerobic training in patients with mitochondrial myopathies Neurology 50 1998 1055 1060
6. T. Taivassalo, J.L. Gardner, and R.W. Taylor Endurance training and detraining in mitochondrial myopathies due to single large-scale mtDNA deletions Brain 129 2006 3391 3401
7. P. Cejudo, J. Bautista, and T. Montemayor Exercise training in mitochondrial myopathy: a randomized controlled trial Muscle Nerve 32 2005 342 350
8. T.D. Jeppesen, M. Schwartz, and D.B. Olsen Aerobic training is safe and improves exercise capacity in patients with mitochondrial myopathy Brain 129 2006 3402 3412
9. J.L. Murphy, E.L. Blakely, and A.M. Schaefer Resistance training in patients with single, large-scale deletions of mitochondrial DNA Brain 131 2008 2832 2840
10. M. Hirano, and S.G. Pavlakis Mitochondrial myopathy, encephalopathy, lactic acidosis, and strokelike episodes (MELAS): current concepts J Child Neurol 9 1994 4 13
11. R. Anan, M. Nakagawa, and M. Miyata Cardiac involvement in mitochondrial diseases. A study on 17 patients with documented mitochondrial DNA defects Circulation 91 1995 955 961
12. K. Majamaa-Voltti, K. Peuhkurinen, M.L. Kortelainen, I.E. Hassinen, and K. Majamaa Cardiac abnormalities in patients with mitochondrial DNA mutation 3243A>G BMC Cardiovasc Disord 2 2002 12
13. D. Holmgren, H. Wahlander, B. Eriksson, A. Oldfors, E. Holme, and M. Tulinius Cardiomyopathy in children with mitochondrial disease; clinical course and cardiological findings Eur Heart J 24 2003 280 288
14. T.C.G. Vydt, R.F.M. de Coo, and O.I.I. Soliman Cardiac involvement in adults with m.3243A>G MELAS gene mutation Am J Cardiol 99 2007 264 269
15. K. Majamaa-Voltti, J. Turkka, M.L. Kortelainen, H. Huikuri, and K. Majamaa Causes of death in pedigrees with the 3243A>G mutation in mitochondrial DNA J Neurol Neurosurg Psychiatry 79 2008 209 211
16. R. Lodi, B. Rajagopalan, A.M. Blamire, J.G. Crilley, P. Styles, and P.F. Chinnery Abnormal cardiac energetics in patients carrying the A3243G mtDNA mutation measured in vivo using phosphorus MR spectroscopy Biochim Biophys Acta 1657 2004 146 150
17. M.G. Bates, K.G. Hollingsworth, and J.H. Newman Concentric hypertrophic remodelling and subendocardial dysfunction in mitochondrial DNA point mutation carriers Eur Heart J Cardiovasc Imaging 2012 10.1093/ehjci/jes226 (accessed 28th January 2013)
18. S. Neubauer, T. Krahe, and R. Schindler 31P magnetic resonance spectroscopy in dilated cardiomyopathy and coronary artery disease. Altered cardiac high-energy phosphate metabolism in heart failure Circulation 86 1992 1810 1818
19. Y. Momiyama, Y. Suzuki, and M. Ohtomo Cardiac autonomic nervous dysfunction in diabetic patients with a mitochondrial DNA mutation: assessment by heart rate variability Diabetes Care 25 2002 2308 2313
20. K. Majamaa-Voltti, K. Majamaa, K. Peuhkurinen, T.H. Makikallio, and H.V. Huikuri Cardiovascular autonomic regulation in patients with 3243A>G mitochondrial DNA mutation Ann Med 36 2004 225 231
21. J.T. Bigger Jr., J.L. Fleiss, R.C. Steinman, L.M. Rolnitzky, R.E. Kleiger, and J.N. Rottman Frequency domain measures of heart period variability and mortality after myocardial infarction Circulation 85 1992 164 171
22. P.S. Douglas, M.L. O'Toole, S.E. Katz, G.S. Ginsburg, W.D. Hiller, and R.H. Laird Left ventricular hypertrophy in athletes Am J Cardiol 80 1997 1384 1388
23. A. Pelliccia, F. Culasso, F.M. Di Paolo, and B.J. Maron Physiologic left ventricular cavity dilatation in elite athletes Ann Intern Med 130 1999 23 31
24. J. Scharhag, G. Schneider, A. Urhausen, V. Rochette, B. Kramann, and W. Kindermann Athlete's heart: right and left ventricular mass and function in male endurance athletes and untrained individuals determined by magnetic resonance imaging J Am Coll Cardiol 40 2002 1856 1863
25. M. Beer, D. Wagner, and J. Myers Effects of exercise training on myocardial energy metabolism and ventricular function assessed by quantitative phosphorus-31 magnetic resonance spectroscopy and magnetic resonance imaging in dilated cardiomyopathy J Am Coll Cardiol 51 2008 1883 1891
26. K.Q. Stolen, J. Kemppainen, and H. Ukkonen Exercise training improves biventricular oxidative metabolism and left ventricular efficiency in patients with dilated cardiomyopathy J Am Coll Cardiol 41 2003 460 467
27. R. Belardinelli, D. Georgiou, G. Cianci, and A. Purcaro Randomized, controlled trial of long-term moderate exercise training in chronic heart failure: effects on functional capacity, quality of life, and clinical outcome Circulation 99 1999 1173 1182
28. W.L. Beaver, K. Wasserman, and B.J. Whipp A new method for detecting anaerobic threshold by gas exchange J Appl Physiol 60 1986 2020 2027
29. S.G. Williams, G.A. Cooke, and D.J. Wright Peak exercise cardiac power output; a direct indicator of cardiac function strongly predictive of prognosis in chronic heart failure Eur Heart J 22 2001 1496 1503
30. A.M. Schaefer, C. Phoenix, J.L. Elson, R. McFarland, P.F. Chinnery, and D.M. Turnbull Mitochondrial disease in adults: a scale to monitor progression and treatment Neurology 66 2006 1932 1934
31. R.G. Whittaker, J.K. Blackwood, and C.L. Alston Urine heteroplasmy is the best predictor of clinical outcome in the m.3243A>G mtDNA mutation Neurology 72 2009 568 569
32. D.E. Jones, K. Hollingsworth, and G. Fattakhova Impaired cardiovascular function in primary biliary cirrhosis Am J Physiol Gastrointest Liver Physiol 298 2010 G764 G773
33. L. Vanhamme, S. Van Huffel, P. Van Hecke, and D. van Ormondt Time-domain quantification of series of biomedical magnetic resonance spectroscopy signals J Magn Reson 140 1999 120 130
34. J. Lumens, T. Delhaas, T. Arts, B.R. Cowan, and A.A. Young Impaired subendocardial contractile myofiber function in asymptomatic aged humans, as detected using MRI Am J Physiol Heart Circ Physiol 291 2006 H1573 H1579
35. J. Fortin, W. Marte, and R. Grullenberger Continuous non-invasive blood pressure monitoring using concentrically interlocking control loops Comput Biol Med 36 2006 941 957
36. G. Gratze, J. Fortin, and A. Holler A software package for non-invasive, real-time beat-to-beat monitoring of stroke volume, blood pressure, total peripheral resistance and for assessment of autonomic function Comput Biol Med 28 1998 121 142
37. G. Parati, G. Ongaro, and G. Bilo Non-invasive beat-to-beat blood pressure monitoring: new developments Blood Press Monit 8 2003 31 36
38. A.M. Bianchi, L.T. Mainardi, C. Meloni, S. Chierchia, and S. Cerutti Continuous monitoring of the sympatho-vagal balance through spectral analysis IEEE Eng Med Biol Mag 16 1997 64 73
39. H.M. Stauss Heart rate variability Am J Physiol Regul Integr Comp Physiol 285 2003 R927 R931
40. S. Akselrod, D. Gordon, J.B. Madwed, N.C. Snidman, D.C. Shannon, and R.J. Cohen Hemodynamic regulation: investigation by spectral analysis Am J Physiol 249 1985 H867 H875
41. K. Alfakih, S. Plein, H. Thiele, T. Jones, J.P. Ridgway, and M.U. Sivananthan Normal human left and right ventricular dimensions for MRI as assessed by turbo gradient echo and steady-state free precession imaging sequences J Magn Reson Imaging 17 2003 323 329
42. J. Jeppesen, and B. Kiens Regulation and limitations to fatty acid oxidation during exercise J Physiol 590 2012 1059 1068
43. T. Taivassalo, T.D. Jensen, N. Kennaway, S. DiMauro, J. Vissing, and R.G. Haller The spectrum of exercise tolerance in mitochondrial myopathies: a study of 40 patients Brain 126 2003 413 423
44. T. Taivassalo, A. Abbott, P. Wyrick, and R.G. Haller Venous oxygen levels during aerobic forearm exercise: an index of impaired oxidative metabolism in mitochondrial myopathy Ann Neurol 51 2002 38 44
45. T.D. Jensen, P. Kazemi-Esfarjani, E. Skomorowska, and J. Vissing A forearm exercise screening test for mitochondrial myopathy Neurology 58 2002 1533 1538
46. T. Taivassalo, E.A. Shoubridge, and J. Chen Aerobic conditioning in patients with mitochondrial myopathies: physiological, biochemical, and genetic effects Ann Neurol 50 2001 133 141
47. K. Abe, Y. Matsuo, J. Kadekawa, S. Inoue, and T. Yanagihara Measurement of tissue oxygen consumption in patients with mitochondrial myopathy by noninvasive tissue oximetry Neurology 49 1997 837 841
48. W. Bank, and B. Chance Diagnosis of defects in oxidative muscle metabolism by non-invasive tissue oximetry Mol Cell Biochem 174 1997 7 10
49. W. Bank, and B. Chance An oxidative defect in metabolic myopathies: diagnosis by noninvasive tissue oximetry Ann Neurol 36 1994 830 837
50. J. Vissing, H. Galbo, and R.G. Haller Exercise fuel mobilization in mitochondrial myopathy: a metabolic dilemma Ann Neurol 40 1996 655 662
51. M. Ozawa, Y. Goto, R. Sakuta, Y. Tanno, S. Tsuji, and I. Nonaka The 8,344 mutation in mitochondrial DNA: a comparison between the proportion of mutant DNA and clinico-pathologic findings Neuromuscul Disord 5 1995 483 488
52. R.G. Haller, S.F. Lewis, R.W. Estabrook, S. DiMauro, S. Servidei, and D.W. Foster Exercise intolerance, lactic acidosis, and abnormal cardiopulmonary regulation in exercise associated with adult skeletal muscle cytochrome c oxidase deficiency J Clin Invest 84 1989 155 161
53. D.G. Jakovljevic, S.A. Moore, L.B. Tan, L. Rochester, G.A. Ford, and M.I. Trenell Discrepancy between cardiac and physical functional reserves in stroke Stroke 43 2012 1422 1425
54. D.M. Mancini, E. Coyle, and A. Coggan Contribution of intrinsic skeletal muscle changes to 31P NMR skeletal muscle metabolic abnormalities in patients with chronic heart failure Circulation 80 1989 1338 1346
55. D.M. Mancini, G. Walter, and N. Reichek Contribution of skeletal muscle atrophy to exercise intolerance and altered muscle metabolism in heart failure Circulation 85 1992 1364 1373
56. D. Harrington, S.D. Anker, T.P. Chua, K.M. Webb-Peploe, P.P. Ponikowski, P.A. Poole-Wilson, and A.J. Coats Skeletal muscle function and its relation to exercise tolerance in chronic heart failure J Am Coll Cardiol 30 1997 1758 1764
57. T. Troosters, R. Gosselink, and M. Decramer Chronic obstructive pulmonary disease and chronic heart failure: two muscle diseases? J Cardiopulm Rehabil 24 2004 137 145
58. K.G. Hollingsworth, G.S. Gorman, and M.I. Trenell Cardiomyopathy is common in patients with the mitochondrial DNA m.3243A>G mutation and correlates with mutation load Neuromuscul Disord 22 2012 592 596
59. H. Ashrafian, C. Redwood, E. Blair, and H. Watkins Hypertrophic cardiomyopathy: a paradigm for myocardial energy depletion Trends Genet 19 2003 263 268
60. J.G. Crilley, E.A. Boehm, and E. Blair Hypertrophic cardiomyopathy due to sarcomeric gene mutations is characterized by impaired energy metabolism irrespective of the degree of hypertrophy J Am Coll Cardiol 41 2003 1776 1782
61. H.R. Middlekauff Making the case for skeletal myopathy as the major limitation of exercise capacity in heart failure Circ Heart Fail 3 2010 537 546
62. T. Parsons, L. Weimer, and K. Engelstad Autonomic symptoms in carriers of the m.3243A>G mitochondrial DNA mutation Arch Neurol 67 2010 976 979
63. P.D. Syme, F. Brunotte, Y. Green, J.K. Aronson, and G.K. Radda The effect of beta 2-adrenoceptor stimulation and blockade of l-type calcium channels on in vivo Na +/H + antiporter activity in rat skeletal muscle Biochim Biophys Acta 1093 1991 234 240
64. H.R. Middlekauff, M.A. Hamilton, L.W. Stevenson, and A.L. Mark Independent control of skin and muscle sympathetic nerve activity in patients with heart failure Circulation 90 1994 1794 1798
65. G. Grassi, M. Colombo, G. Seravalle, D. Spaziani, and G. Mancia Dissociation between muscle and skin sympathetic nerve activity in essential hypertension, obesity, and congestive heart failure Hypertension 31 1998 64 67
66. D. Hering, Z. Zdrojewski, and E. Krol Tonic chemoreflex activation contributes to the elevated muscle sympathetic nerve activity in patients with chronic renal failure J Hypertens 25 2007 157 161
67. J. Park, V.M. Campese, N. Nobakht, and H.R. Middlekauff Differential distribution of muscle and skin sympathetic nerve activity in patients with end-stage renal disease J Appl Physiol 105 2008 1873 1876
68. A.L. Clark, P.A. Poole-Wilson, and A.J. Coats Exercise limitation in chronic heart failure: central role of the periphery J Am Coll Cardiol 28 1996 1092 1102
69. J. Vissing, U. Gansted, and B. Quistorff Exercise intolerance in mitochondrial myopathy is not related to lactic acidosis Ann Neurol 49 2001 672 676
70. J. Vissing, S.F. Vissing, D.A. MacLean, B. Saltin, B. Quistorff, and R.G. Haller Sympathetic activation in exercise is not dependent on muscle acidosis. Direct evidence from studies in metabolic myopathies J Clin Invest 101 1998 1654 1660
71. S.A. Smith, J.H. Mitchell, and M.G. Garry The mammalian exercise pressor reflex in health and disease Exp Physiol 91 2006 89 102