Effects of short-term treadmill exercise training or growth hormone supplementation on diastolic function and exercise tolerance in old rats

Journals of Gerontology - Series A Biological Sciences and Medical Sciences

Volumn 63, Issue 9, 2008, Pages 911-920

  Groban, Leanne ^a   Jobe, Harrison ^a   Lin, Marina ^a   Houle, Timothy ^a   Kitzman, Dalane A ^a   Sonntag, William ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Aging; Diastolic function; Growth hormone; Insulin like growth factor 1; Treadmill training

Indexed keywords

ANGIOTENSIN; GROWTH HORMONE; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; SOMATOMEDIN C;

ANIMAL EXPERIMENT; ARTICLE; BIOCHEMISTRY; CONTROLLED STUDY; ENZYME REGULATION; EXERCISE TOLERANCE; HEART FUNCTION; HEART MUSCLE; MALE; MUSCLE RELAXATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SUPPLEMENTATION; TREADMILL EXERCISE;

ANIMALIA; RATTUS; RATTUS NORVEGICUS;

EID: 54249147501     PISSN: 10795006     EISSN: None     Source Type: Journal    
DOI: 10.1093/gerona/63.9.911     Document Type: Article

References (80)

1. Higginbotham MB, Morris KG, Williams RS, Coleman RE, Cobb FR. Physiologic basis for the age-related decline in aerobic work capacity. Am J Cardiol. 1986;57:1374-1379.
2. Schulman SP, Lakatta EG, Fleg JL, Lakatta L, Becker LC, Gerstenblith G. Age-related decline in left ventricular filling at rest and exercise. Am J Physiol. 1992;263(6 Pt 2):H1932-H1938.
3. Groban L. Diastolic dysfunction in the older heart. J Cardiothorac Vasc Anesth. 2005;19:228-236.
4. Little WC, Kitzman DW, Cheng CP. Diastolic dysfunction as a cause of exercise intolerance. Heart Fail Rev. 2000;5:301-306.
5. Kitzman DW, Higginbotham MB, Cobb FR, Sheikh KH, Sullivan MJ. Exercise intolerance in patients with heart failure and preserved left ventricular systolic function: failure of the Frank-Starling mechanism. J Am Coll Cardiol. 1991;17:1065-1072.
6. Kitzman DW, Little WC, Brubaker PH, et al. Pathophysiological characterization of isolated diastolic heart failure in comparison to systolic heart failure. JAMA. 2002;288:2144-2150.
7. Brenner DA, Apstein CS, Saupe KW. Exercise training attenuates age-associated diastolic dysfunction in rats. Circulation. 2001;104:221-226.
8. Forman DE, Manning WJ, Hauser R, Gervino EV, Evans WJ, Wei JY. Enhanced left ventricular diastolic filling associated with long-term endurance training. J Gerontol. 1992;47:M56-M58.
9. Levy WC, Cerqueira MD, Abrass IB, Schwartz RS, Stratton JR. Endurance exercise training augments diastolic filling at rest and during exercise in healthy young and older men. Circulation. 1993;88:116-126.
10. Li Y, Lincoln T, Mendelowitz D, Grossman W, Wei JY. Age-related differences in effect of exercise training on cardiac muscle function in rats. Am J Physiol. 1986;251(1 Pt 2):H12-H18.
11. Starnes JW, Beyer RE, Edington DW. Myocardial adaptations to endurance exercise in aged rats. Am J Physiol. 1983;245:H560-H566.
12. Takemoto KA, Bernstein L, Lopez JF, Marshak D, Rahimtoola SH, Chandraratna PA. Abnormalities of diastolic filling of the left ventricle associated with aging are less pronounced in exercise-trained individuals. Am Heart J. 1992;124:143-148.
13. Tate CA, Taffet GE, Hudson EK, Blaylock SL, McBride RP, Michael LH. Enhanced calcium uptake of cardiac sarcoplasmic reticulum in exercise-trained old rats. Am J Physiol. 1990;258(2 Pt 2):H431-H435.
14. Tate CA, Helgason T, Hyek MF, et al. SERCA2a and mitochondrial cytochrome oxidase expression are increased in hearts of exercise-trained old rats. Am J Physiol. 1996;271(1 Pt 2):H68-H72.
15. Thomas DP, Zimmerman SD, Hansen TR, Martin DT, McCormick RJ. Collagen gene expression in rat left ventricle: interactive effect of age and exercise training. J Appl Physiol. 2000;89:1462-1468.
16. Blomqvist CG, Saltin B. Cardiovascular adaptations to physical training. Annu Rev Physiol. 1983;45:169-189.
17. Bloor CM, Leon AS. Interaction of age and exercise on the heart and its blood supply. Lab Invest. 1970;22:160-165.
18. Gates PE, Tanaka H, Graves J, Seals DR. Left ventricular structure and diastolic function with human ageing. Relation to habitual exercise and arterial stiffness. Eur Heart J. 2003;24:2213-2220.
19. Iemitsu M, Miyauchi T, Maeda S, et al. Exercise training improves cardiac function-related gene levels through thyroid hormone receptor signaling in aged rats. Am J Physiol Heart Circ Physiol. 2004;286:H1696-H1705.
20. Tanaka H, Dinenno FA, Monahan KD, Clevenger CM, DeSouza CA, Seals DR. Aging, habitual exercise, and dynamic arterial compliance. Circulation. 2000;102:1270-1275.
21. Khan AS, Sane DC, Wannenburg T, Sonntag WE. Growth hormone, insulin-like growth factor-1 and the aging cardiovascular system. Cardiovasc Res. 2002;54:25-35.
22. Colao A, Cuocolo A, Di Somma C, et al. Impaired cardiac performance in elderly patients with growth hormone deficiency. J Clin Endocrinol Metab. 1999;84:3950-3955.
23. Colao A, di Somma C, Pivonello R, et al. The cardiovascular risk of adult GH deficiency (GHD) improved after GH replacement and worsened in untreated GHD: a 12-month prospective study. J Clin Endocrinol Metab. 2002;87:1088-1093.
24. Colao A, Vitale G, Pivonello R, Ciccarelli A, Di Somma C, Lombardi G. The heart: an end-organ of GH action. Eur J Endocrinol. 2004;151(Suppl 1):S93-S101.
25. Vasan RS, Sullivan LM, D'Agostino RB, et al. Serum insulin-like growth factor I and risk for heart failure in elderly individuals without a previous myocardial infarction: the Framingham Heart Study. Ann Intern Med. 2003;139:642-648.
26. Wannenburg T, Khan AS, Sane DC, Willingham MC, Faucette T, Sonntag WE. Growth hormone reverses age-related cardiac myofilament dysfunction in rats. Am J Physiol Heart Circ Physiol. 2001;281:H915-H922.
27. Woodhouse LJ, Mukherjee A, Shalet SM, Ezzat S. The influence of growth hormone status on physical impairments, functional limitations, and health-related quality of life in adults. Endocr Rev. 2006;27:287-317.
28. Groban L, Pailes NA, Bennett CD, et al. Growth hormone replacement attenuates diastolic dysfunction and cardiac angiotensin II expression in senescent rats. J Gerontol A Biol Sci Med Sci. 2006;61:28-35.
29. Hurel SJ, Koppiker N, Newkirk J, et al. Relationship of physical exercise and ageing to growth hormone production. Clin Endocrinol (Oxf). 1999;51:687-691.
30. Poehlman ET, Copeland KC. Influence of physical activity on insulinlike growth factor-I in healthy younger and older men. J Clin Endocrinol Metab. 1990;71:1468-1473.
31. Sonntag WE, Steger RW, Forman LJ, Meites J. Decreased pulsatile release of growth hormone in old male rats. Endocrinology. 1980;107:1875-1879.
32. Corpas E, Harman SM, Blackman MR. Human growth hormone and human aging. Endocr Rev. 1993;14:20-39.
33. Rudman D, Feller AG, Nagraj HS, et al. Effects of human growth hormone in men over 60 years old. N Engl J Med. 1990;323:1-6.
34. McMurray J. Renin angiotensin blockade in heart failure with preserved ejection fraction: the signal gets stronger. Eur Heart J. 2006;27:2257-2259.
35. Sahn DJ, DeMaria A, Kisslo J, Weyman A. Recommendations regarding quantitation in M-mode echocardiography: results of a survey of echocardiographic measurements. Circulation. 1978;58:1072-1083.
36. Daughaday WH, Parker KA, Borowsky S, Trivedi B, Kapadia M. Measurement of somatomedin-related peptides in fetal, neonatal, and maternal rat serum by insulin-like growth factor (IGF) I RIA, IGF-II radioreceptor assay (RRA), and multiplication-stimulating activity RRA after acid-ethanol extraction. Endocrinology. 1982;110:575-581.
37. Sonntag WE, Lenham JE, Ingram RL. Effects of aging and dietary restriction on tissue protein synthesis: relationship to plasma insulin-like growth factor-1. J Gerontol. 1992;47:B159-B163.
38. Cohn J. Statistical Power Analysis for Behavioral Sciences, 4th Ed. Mahwah, NJ: Lawrence Erlbaum Associates; 1998.
39. Dimke H, Flyvbjerg A, Frische S. Acute and chronic effects of growth hormone on renal regulation of electrolyte and water homeostasis. Growth Horm IGF Res. 2007;17:353-368.
40. Kitzman DW, Gardin JM, Gottdiener JS, et al. Importance of heart failure with preserved systolic function in patients > or = 65 years of age. Am J Cardiol. 2001;87:413-419.
41. Carro E, Nuñez A, Busiguina S, Torres-Aleman I. Circulating insulin-like growth factor I mediates effects of exercise on the brain. J Neurosci. 2000;20:2926-2933.
42. Eliakim A, Moromisato M, Moromisato D, Brasel JA, Roberts C Jr, Cooper DM. Increase in muscle IGF-I protein but not IGF-I mRNA after 5 days of endurance training in young rats. Am J Physiol. 1997;273(4 Pt 2):R1557-R1561.
43. Gillespie CM, Merkel AL, Martin AA. Effects of insulin-like growth factor-I and LR3IGF-I on regional blood flow in normal rats. J Endocrinol. 1997;155:351-358.
44. Deley G, Kervio G, Van Hoecke J, Verges B, Grassi B, Casillas JM. Effects of a one-year exercise training program in adults over 70 years old: a study with a control group. Aging Clin Exp Res. 2007;19:310-315.
45. Smart N, Haluska B, Jeffriess L, Marwick TH. Exercise training in systolic and diastolic dysfunction: effects on cardiac function, functional capacity, and quality of life. Am Heart J. 2007;153:530-536.
46. Baldi JC, McFarlane K, Oxenham HC, Whalley GA, Walsh HJ, Doughty RN. Left ventricular diastolic filling and systolic function of young and older trained and untrained men. J Appl Physiol. 2003;95:2570-2575.
47. Fleg JL, Shapiro EP, O'Connor F, Taube J, Goldberg AP, Lakatta EG. Left ventricular diastolic filling performance in older male athletes. JAMA. 1995;273:1371-1375.
48. Nottin S, Nguyen LD, Terbah M, Obert P. Long-term endurance training does not prevent the age-related decrease in left ventricular relaxation properties. Acta Physiol Scand. 2004;181:209-215.
49. Schmidt-Trucksäss A, Schmid A, Häussler C, Huber G, Huonker M, Keul J. Left ventricular wall motion during diastolic filling in endurance-trained athletes. Med Sci Sports Exerc. 2001;33:189-195.
50. Manetta J, Brun JF, Maimoun L, Callis A, Préfaut C, Mercier J. Effect of training on the GH/IGF-I axis during exercise in middle-aged men: relationship to glucose homeostasis. Am J Physiol Endocrinol Metab. 2002;283:E929-E936.
51. Bermon S, Ferrari P, Bernard P, Altare S, Dolisi C. Responses of total and free insulin-like growth factor-I and insulin-like growth factor binding protein-3 after resistance exercise and training in elderly subjects. Acta Physiol Scand. 1999;165:51-56.
52. Kraemer WJ, Aguilera BA, Terada M, et al. Responses of IGF-I to endogenous increases in growth hormone after heavy-resistance exercise. J Appl Physiol. 1995;79:1310-1315.
53. Heo YR, King CW. Influence of exercise-training on insulin-like growth factor I and II in rats. Nutr Res. 2001;21:1191-1199.
54. Gomes RJ, de Mello MA, Caetano FH, et al. Effects of swimming training on bone mass and the GH/IGF-1 axis in diabetic rats. Growth Horm IGF Res. 2006;16:326-331.
55. Scheinowitz M, Kessler-Icekson G, Freimann S, et al. Short- and long-term swimming exercise training increases myocardial insulin-like growth factor-I gene expression. Growth Horm IGF Res. 2003;13:19-25.
56. Ren J, Samson WK, Sowers JR. Insulin-like growth factor I as a cardiac hormone: physiological and pathophysiological implications in heart disease. J Mol Cell Cardiol. 1999;31:2049-2061.
57. Li Q, Wu S, Li SY, et al. Cardiac-specific overexpression of insulin-like growth factor 1 attenuates aging-associated cardiac diastolic contractile dysfunction and protein damage. Am J Physiol Heart Circ Physiol. 2007;292:H1398-H1403.
58. Giannuzzi P, Temporelli PL, Corrà U, Tavazzi L; ELVD-CHF Study Group. Antiremodeling effect of long-term exercise training in patients with stable chronic heart failure: results of the Exercise in Left Ventricular Dysfunction and Chronic Heart Failure (ELVD-CHF) trial. Circulation. 2003;108:554-559.
59. Anker SD, Volterrani M, Pflaum CD, et al. Acquired growth hormone resistance in patients with chronic heart failure: implications for therapy with growth hormone. J Am Coll Cardiol. 2001;38:443-452.
60. Longobardi S, Cittadini A, Strömer H, et al. Echocardiographic assessment of cardiac morphology and function in mutant dwarf rats. Growth Horm IGF Res. 2000;10:242-247.
61. Trask AJ, Ferrario CM. Angiotensin-(1-7): pharmacology and new perspectives in cardiovascular treatments. Cardiovasc Drug Rev. 2007;25:162-174.
62. Cittadini A, Grossman JD, Napoli R, et al. Growth hormone attenuates early left ventricular remodeling and improves cardiac function in rats with large myocardial infarction. J Am Coll Cardiol. 1997;29:1109-1116.
63. Isgaard J, Kujacic V, Jennische E, et al. Growth hormone improves cardiac function in rats with experimental myocardial infarction. Eur J Clin Invest. 1997;27:517-525.
64. Adamopoulos S, Parissis JT, Paraskevaidis I, et al. Effects of growth hormone on circulating cytokine network, and left ventricular contractile performance and geometry in patients with idiopathic dilated cardiomyopathy. Eur Heart J. 2003;24:2186-2196.
65. Parissis JT, Adamopoulos S, Karatzas D, Paraskevaidis J, Livanis E, Kremastinos D. Growth hormone-induced reduction of soluble apoptosis mediators is associated with reverse cardiac remodelling and improvement of exercise capacity in patients with idiopathic dilated cardiomyopathy. Eur J Cardiovasc Prev Rehabil. 2005;12:164-168.
66. Brüel A, Oxlund H. The effect of growth hormone on rat myocardial collagen. Growth Horm IGF Res. 1999;9:123-130.
67. Cao N, Lau S, Nguyen TT, White PJ. Characterization of the acute cardiovascular effects of intravenously administered insulin-like growth factor-I in conscious Sprague-Dawley rats. Clin Exp Pharmacol Physiol. 2006;33:1190-1195.
68. Lacolley P, Safar ME, Lucet B, Ledudal K, Labat C, Benetos A. Prevention of aortic and cardiac fibrosis by spironolactone in old normotensive rats. J Am Coll Cardiol. 2001;37:662-667.
69. Sadoshima J, Izumo S. Molecular characterization of angiotensin II-induced hypertrophy of cardiac myocytes and hyperplasia of cardiac fibroblasts. Critical role of the AT1 receptor subtype. Circ Res. 1993;73:413-423.
70. Schorb W, Booz GW, Dostal DE, Conrad KM, Chang KC, Baker KM. Angiotensin II is mitogenic in neonatal rat cardiac fibroblasts. Circ Res. 1993;72:1245-1254.
71. Sun Y, Zhang J, Lu L, Bedigian MP, Robinson AD, Weber KT. Tissue angiotensin II in the regulation of inflammatory and fibrogenic components of repair in the rat heart. J Lab Clin Med. 2004;143:41-51.
72. Crackower MA, Sarao R, Oudit GY, et al. Angiotensin-converting enzyme 2 is an essential regulator of heart function. Nature. 2002;417:822-828.
73. Lijnen PJ, Petrov VV. Role of intracardiac renin-angiotensin-aldosterone system in extracellular matrix remodeling. Methods Find Exp Clin Pharmacol. 2003;25:541-564.
74. Trask AJ, Averill DB, Ganten D, Chappell MC, Ferrario CM. Primary role of angiotensin-converting enzyme-2 in cardiac production of angiotensin-(1-7) in transgenic Ren-2 hypertensive rats. Am J Physiol Heart Circ Physiol. 2007;292:H3019-H3024.
75. Nishimura RA, Tajik AJ. Evaluation of diastolic filling of left ventricle in health and disease: Doppler echocardiography is the clinician's Rosetta Stone. J Am Coll Cardiol. 1997;30:8-18.
76. Garcia MJ, Thomas JD, Klein AL. New Doppler echocardiographic applications for the study of diastolic function. J Am Coll Cardiol. 1998;32:865-875.
77. Ommen SR, Nishimura RA, Appleton CP, et al. Clinical utility of Doppler echocardiography and tissue Doppler imaging in the estimation of left ventricular filling pressures: a comparative simultaneous Doppler- catheterization study. Circulation. 2000;102:1788-1794.
78. Kasner M, Westermann D, Steendijk P, et al. Utility of Doppler echocardiography and tissue Doppler imaging in the estimation of diastolic function in heart failure with normal ejection fraction: a comparative Doppler-conductance catheterization study. Circulation. 2007;116:637-647.
79. Liu H, Bravata DM, Olkin I, et al. Systematic review: the safety and efficacy of growth hormone in the healthy elderly. Ann Intern Med. 2007;146:104-115.
80. Tripkovic I, Tripkovic A, Strnad M, Capkun V, Zekan L. Role of insulin-like growth factor-1 in colon cancerogenesis: a case-control study. Arch Med Res. 2007;38:519-525.