Diabetes Mellitus and Exercise Physiology in the Presence of Diabetic Comorbidities

  • Amy G. Huebschmann
  • Judith G. Regensteiner
Chapter
Part of the Contemporary Diabetes book series (CDI)

Abstract

While uncomplicated type 2 diabetes mellitus (T2DM) is already associated with an impaired exercise capacity, the presence of other comorbidities appears to further worsen exercise capacity in T2DM. Common diabetic comorbidities such as hypertension, arterial stiffness, cardiovascular disease, systolic dysfunction, diastolic dysfunction, and diabetic nephropathy are all associated with worse exercise capacity in T2DM. Benefits of exercise training programs for those with T2DM and certain comorbidities (e.g., hypertension, increased arterial stiffness, or post-myocardial infarction) have been shown to include improved exercise capacity. Further study is warranted to determine the specific benefits and risks of exercise training in subpopulations of T2DM such as those with T2DM and either congestive heart failure or microvascular complications of diabetes.

Keywords

Diabetes mellitus Exercise capacity Hypertension Arterial stiffness Cardiovascular disease Diabetic microvascular complications 

Reference

  1. 1.
    Schneider, SH, Khachadurian, AK, Amorosa, LF, Clemow, L, Ruderman, NB: Ten-year experience with an exercise-based outpatient life-style modification program in the treatment of diabetes mellitus. Diabetes Care 15:1800–1810, 1992PubMedGoogle Scholar
  2. 2.
    Kjaer, M, Hollenbeck, CB, Frey-Hewitt, B, Galbo, H, Haskell, W, Reaven, GM: Glucoregulation and hormonal responses to maximal exercise in non-insulin-dependent diabetes. J Appl Physiol 68:2067–2074, 1990PubMedGoogle Scholar
  3. 3.
    Regensteiner, JG, Sippel, J, McFarling, ET, Wolfel, EE, Hiatt, WR: Effects of non-insulin-dependent diabetes on oxygen consumption during treadmill exercise. Med Sci Sports Exerc 27:875–881, 1995PubMedGoogle Scholar
  4. 4.
    Regensteiner, JG, Bauer, TA, Reusch, JE, Brandenburg, SL, Sippel, JM, Vogelsong, AM, Smith, S, Wolfel, EE, Eckel, RH, Hiatt, WR: Abnormal oxygen uptake kinetic responses in women with type II diabetes mellitus. J Appl Physiol 85:310–317, 1998PubMedGoogle Scholar
  5. 5.
    Estacio, RO, Regensteiner, JG, Wolfel, EE, Jeffers, B, Dickenson, M, Schrier, RW: The association between diabetic complications and exercise capacity in NIDDM patients. Diabetes Care 21:291–295, 1998PubMedGoogle Scholar
  6. 6.
    Albright, A, Franz, M, Hornsby, G, Kriska, A, Marrero, D, Ullrich, I, Verity, LS: American College of Sports Medicine position stand. Exercise and type 2 diabetes. Med Sci Sports Exerc 32:1345–1360, 2000PubMedGoogle Scholar
  7. 7.
    Geiss, LS, Rolka, DB, Engelgau, MM: Elevated blood pressure among U.S. adults with diabetes, 1988–1994. Am J Prev Med 22:42–48, 2002PubMedGoogle Scholar
  8. 8.
    Hypertension in Diabetes Study (HDS): I. Prevalence of hypertension in newly presenting type 2 diabetic patients and the association with risk factors for cardiovascular and diabetic complications. J Hypertens 11:309–317, 1993Google Scholar
  9. 9.
    Nichols, GA, Hillier, TA, Erbey, JR, Brown, JB: Congestive heart failure in type 2 diabetes: prevalence, incidence, and risk factors. Diabetes Care 24:1614–1619, 2001PubMedGoogle Scholar
  10. 10.
    Anand, DV, Lim, E, Hopkins, D, Corder, R, Shaw, LJ, Sharp, P, Lipkin, D, Lahiri, A: Risk stratification in uncomplicated type 2 diabetes: prospective evaluation of the combined use of coronary artery calcium imaging and selective myocardial perfusion scintigraphy. Eur Heart J 27:713–721, 2006PubMedGoogle Scholar
  11. 11.
    Fein, F, Scheur, J: Heart disease in diabetes mellitus: theory and practice. Rifkin H, Porte D Jr.s. New York, Elsevier, 1990, pp. 812–823Google Scholar
  12. 12.
    Adler, AI, Stevens, RJ, Neil, A, Stratton, IM, Boulton, AJ, Holman, RR: UKPDS 59: hyperglycemia and other potentially modifiable risk factors for peripheral vascular disease in type 2 diabetes. Diabetes Care 25:894–899, 2002PubMedGoogle Scholar
  13. 13.
    Adler, AI, Stevens, RJ, Manley, SE, Bilous, RW, Cull, CA, Holman, RR: Development and progression of nephropathy in type 2 diabetes: the United Kingdom Prospective Diabetes Study (UKPDS 64). Kidney Int 63:225–232, 2003PubMedGoogle Scholar
  14. 14.
    Brown, JB, Pedula, KL, Summers, KH: Diabetic retinopathy: contemporary prevalence in a well-controlled population. Diabetes Care 26:2637–2642, 2003PubMedGoogle Scholar
  15. 15.
    Veves, A, Saouaf, R, Donaghue, VM, Mullooly, CA, Kistler, JA, Giurini, JM, Horton, ES, Fielding, RA: Aerobic exercise capacity remains normal despite impaired endothelial function in the micro- and macrocirculation of physically active IDDM patients. Diabetes 46:1846–1852, 1997PubMedGoogle Scholar
  16. 16.
    Rowland, TW, Martha, PM, Jr., Reiter, EO, Cunningham, LN: The influence of diabetes mellitus on cardiovascular function in children and adolescents. Int J Sports Med 13:431–435, 1992PubMedGoogle Scholar
  17. 17.
    Regensteiner, JG: Type 2 diabetes mellitus and cardiovascular exercise performance. Rev Endocr Metab Disord 5:269–276, 2004PubMedGoogle Scholar
  18. 18.
    Regensteiner, JG, Groves, BM, Bauer, TA, Reusch, JEB, Smith, SC, Wolfel, EE: Recently diagnosed type 2 diabetes mellitus adversely affects cardiac function during exercise (abstract). Diabetes 51(Suppl. 2):A59, 2002Google Scholar
  19. 19.
    Poirier, P, Garneau, C, Bogaty, P, Nadeau, A, Marois, L, Brochu, C, Gingras, C, Fortin, C, Jobin, J, Dumesnil, JG: Impact of left ventricular diastolic dysfunction on maximal treadmill performance in normotensive subjects with well-controlled type 2 diabetes mellitus. Am J Cardiol 85:473–477, 2000PubMedGoogle Scholar
  20. 20.
    Devereux, RB, Roman, MJ, Paranicas, M, O'Grady, MJ, Lee, ET, Welty, TK, Fabsitz, RR, Robbins, D, Rhoades, ER, Howard, BV: Impact of diabetes on cardiac structure and function: the strong heart study. Circulation 101:2271–2276, 2000PubMedGoogle Scholar
  21. 21.
    Raber, W, Raffesberg, W, Waldhausl, W, Gasic, S, Roden, M: Exercise induces excessive normetanephrine responses in hypertensive diabetic patients. Eur J Clin Invest 33:480–487, 2003PubMedGoogle Scholar
  22. 22.
    Babalola, RO, Ajayi, AA: A cross-sectional study of echocardiographic indices, treadmill exercise capacity and microvascular complications in Nigerian patients with hypertension associated with diabetes mellitus. Diabet Med 9:899–903, 1992PubMedGoogle Scholar
  23. 23.
    Esler, M: The sympathetic system and hypertension. Am J Hypertens 13:99S–105S, 2000PubMedGoogle Scholar
  24. 24.
    Esler, M, Rumantir, M, Kaye, D, Lambert, G: The sympathetic neurobiology of essential hypertension: disparate influences of obesity, stress, and noradrenaline transporter dysfunction? Am J Hypertens 14:139S–146S, 2001PubMedGoogle Scholar
  25. 25.
    Esler, M, Rumantir, M, Wiesner, G, Kaye, D, Hastings, J, Lambert, G: Sympathetic nervous system and insulin resistance: from obesity to diabetes. Am J Hypertens 14:304S–309S, 2001PubMedGoogle Scholar
  26. 26.
    Johnson, RJ, Rodriguez-Iturbe, B, Kang, DH, Feig, DI, Herrera-Acosta, J: A unifying pathway for essential hypertension. Am J Hypertens 18:431–440, 2005PubMedGoogle Scholar
  27. 27.
    Christensen, NJ, Galbo, H: Sympathetic nervous activity during exercise. Annu Rev Physiol 45:139–153, 1983PubMedGoogle Scholar
  28. 28.
    Sullivan, L: Obesity, diabetes mellitus and physical activity – metabolic responses to physical training in adipose and muscle tissues. Ann Clin Res 14(Suppl. 34):51–62, 1982PubMedGoogle Scholar
  29. 29.
    Goldstein, DS: Plasma catecholamines and essential hypertension. An analytical review. Hypertension 5:86–99, 1983PubMedGoogle Scholar
  30. 30.
    Goldstein, DS: Plasma norepinephrine during stress in essential hypertension. Hypertension 3:551–556, 1981PubMedGoogle Scholar
  31. 31.
    Zinman, B, Ruderman, N, Campaigne, BN, Devlin, JT, Schneider, SH: Physical activity/exercise and diabetes. Diabetes Care 27(Suppl. 1):S58–S62, 2004Google Scholar
  32. 32.
    Et-Taouil, K, Safar, M, Plante, GE: Mechanisms and consequences of large artery rigidity. Can J Physiol Pharmacol 81:205–211, 2003PubMedGoogle Scholar
  33. 33.
    Nichols, WW, O'Rourke, M: McDonald's blood flow in arteries: theoretical, experimental and clinical principles. 2005. London, UK.Google Scholar
  34. 34.
    Mitchell, GF, Lacourciere, Y, Ouellet, JP, Izzo, JL, Jr., Neutel, J, Kerwin, LJ, Block, AJ, Pfeffer, MA: Determinants of elevated pulse pressure in middle-aged and older subjects with uncomplicated systolic hypertension: the role of proximal aortic diameter and the aortic pressure-flow relationship. Circulation 108:1592–1598, 2003PubMedGoogle Scholar
  35. 35.
    Chobanian, AV, Bakris, GL, Black, HR, Cushman, WC, Green, LA, Izzo, JL, Jr., Jones, DW, Materson, BJ, Oparil, S, Wright, JT, Jr., Roccella, EJ: The Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure: the JNC 7 report. JAMA 289:2560–2572, 2003PubMedGoogle Scholar
  36. 36.
    Williams, B, Lacy, PS, Thom, SM, Cruickshank, K, Stanton, A, Collier, D, Hughes, AD, Thurston, H, O'Rourke, M: Differential impact of blood pressure-lowering drugs on central aortic pressure and clinical outcomes: principal results of the Conduit Artery Function Evaluation (CAFE) study. Circulation 113:1213–1225, 2006PubMedGoogle Scholar
  37. 37.
    Franzeck, UK, Talke, P, Bernstein, EF, Golbranson, FL, Fronek, A: Transcutaneous PO2 measurements in health and peripheral arterial occlusive disease. Surgery 91:156–163, 1982PubMedGoogle Scholar
  38. 38.
    Wyss, CR, Matsen, FA, III, Simmons, CW, Burgess, EM: Transcutaneous oxygen tension measurements on limbs of diabetic and nondiabetic patients with peripheral vascular disease. Surgery 95:339–346, 1984PubMedGoogle Scholar
  39. 39.
    Rooke, TW, Osmundson, PJ: The influence of age, sex, smoking, and diabetes on lower limb transcutaneous oxygen tension in patients with arterial occlusive disease. Arch Intern Med 150:129–132, 1990PubMedGoogle Scholar
  40. 40.
    Kizu, A, Koyama, H, Tanaka, S, Maeno, T, Komatsu, M, Fukumoto, S, Emoto, M, Shoji, T, Inaba, M, Shioi, A, Miki, T, Nishizawa, Y: Arterial wall stiffness is associated with peripheral circulation in patients with type 2 diabetes. Atherosclerosis 170:87–91, 2003PubMedGoogle Scholar
  41. 41.
    Matthys, D, Craen, M, De Wolf, D, Vande, WJ, Verhaaren, H: Reduced decrease of peripheral vascular resistance during exercise in young type I diabetic patients. Diabetes Care 19:1286–1288, 1996PubMedGoogle Scholar
  42. 42.
    Rubler, S, Arvan, SB: Exercise testing in young asymptomatic diabetic patients. Angiology 27:539–548, 1976PubMedGoogle Scholar
  43. 43.
    Newkumet, KM, Goble, MM, Young, RB, Kaplowitz, PB, Schieken, RM: Altered blood pressure reactivity in adolescent diabetics. Pediatrics 93:616–621, 1994PubMedGoogle Scholar
  44. 44.
    Whelton, SP, Chin, A, Xin, X, He, J: Effect of aerobic exercise on blood pressure: a meta-analysis of randomized, controlled trials. Ann Intern Med 136:493–503, 2002PubMedGoogle Scholar
  45. 45.
    Kelley, GA, Kelley, KA, Tran, ZV: Aerobic exercise and resting blood pressure: a meta-analytic review of randomized, controlled trials. Prev Cardiol 4:73–80, 2001PubMedGoogle Scholar
  46. 46.
    Kelley, GA, Kelley, KS, Tran, ZV: Walking and resting blood pressure in adults: a meta-analysis. Prev Med 33:120–127, 2001PubMedGoogle Scholar
  47. 47.
    Turner, MJ, Spina, RJ, Kohrt, WM, Ehsani, AA: Effect of endurance exercise training on left ventricular size and remodeling in older adults with hypertension. J Gerontol A Biol Sci Med Sci 55:M245–M251, 2000PubMedGoogle Scholar
  48. 48.
    Domanski, M, Mitchell, G, Pfeffer, M, Neaton, JD, Norman, J, Svendsen, K, Grimm, R, Cohen, J, Stamler, J: Pulse pressure and cardiovascular disease-related mortality: follow-up study of the Multiple Risk Factor Intervention Trial (MRFIT). JAMA 287:2677–2683, 2002PubMedGoogle Scholar
  49. 49.
    Benetos, A, Thomas, F, Bean, K, Gautier, S, Smulyan, H, Guize, L: Prognostic value of systolic and diastolic blood pressure in treated hypertensive men. Arch Intern Med 162:577–581, 2002PubMedGoogle Scholar
  50. 50.
    Turnbull, F: Effects of different blood-pressure-lowering regimens on major cardiovascular events: results of prospectively-designed overviews of randomised trials. Lancet 362:1527–1535, 2003PubMedGoogle Scholar
  51. 51.
    Levy, D, Salomon, M, D'Agostino, RB, Belanger, AJ, Kannel, WB: Prognostic implications of baseline electrocardiographic features and their serial changes in subjects with left ventricular hypertrophy. Circulation 90:1786–1793, 1994PubMedGoogle Scholar
  52. 52.
    Mathew, J, Sleight, P, Lonn, E, Johnstone, D, Pogue, J, Yi, Q, Bosch, J, Sussex, B, Probstfield, J, Yusuf, S: Reduction of cardiovascular risk by regression of electrocardiographic markers of left ventricular hypertrophy by the angiotensin-converting enzyme inhibitor ramipril. Circulation 104:1615–1621, 2001PubMedGoogle Scholar
  53. 53.
    Devereux, RB, Wachtell, K, Gerdts, E, Boman, K, Nieminen, MS, Papademetriou, V, Rokkedal, J, Harris, K, Aurup, P, Dahlof, B: Prognostic significance of left ventricular mass change during treatment of hypertension. JAMA 292:2350–2356, 2004PubMedGoogle Scholar
  54. 54.
    Menard, J, Payette, H, Baillargeon, JP, Maheux, P, Lepage, S, Tessier, D, Ardilouze, JL: Efficacy of intensive multitherapy for patients with type 2 diabetes mellitus: a randomized controlled trial. CMAJ 173:1457–1466, 2005PubMedGoogle Scholar
  55. 55.
    Woodiwiss, AJ, Kalk, WJ, Norton, GR: Habitual exercise attenuates myocardial stiffness in diabetes mellitus in rats. Am J Physiol 271:H2126–H2133, 1996PubMedGoogle Scholar
  56. 56.
    Yokoyama, H, Emoto, M, Fujiwara, S, Motoyama, K, Morioka, T, Koyama, H, Shoji, T, Inaba, M, Nishizawa, Y: Short-term aerobic exercise improves arterial stiffness in type 2 diabetes. Diabetes Res Clin Pract 65:85–93, 2004PubMedGoogle Scholar
  57. 57.
    Ferrier, KE, Waddell, TK, Gatzka, CD, Cameron, JD, Dart, AM, Kingwell, BA: Aerobic exercise training does not modify large-artery compliance in isolated systolic hypertension. Hypertension 38:222–226, 2001PubMedGoogle Scholar
  58. 58.
    Rubler, S, Dlugash, J, Yuceoglu, YZ, Kumral, T, Branwood, AW, Grishman, A: New type of cardiomyopathy associated with diabetic glomerulosclerosis. Am J Cardiol 30:595–602, 1972PubMedGoogle Scholar
  59. 59.
    Di Bonito, P, Cuomo, S, Moio, N, Sibilio, G, Sabatini, D, Quattrin, S, Capaldo, B: Diastolic dysfunction in patients with non-insulin-dependent diabetes mellitus of short duration. Diabet Med 13:321–324, 1996PubMedGoogle Scholar
  60. 60.
    Beljic, T, Miric, M: Improved metabolic control does not reverse left ventricular filling abnormalities in newly diagnosed non-insulin-dependent diabetes patients. Acta Diabetol 31:147–150, 1994PubMedGoogle Scholar
  61. 61.
    Nicolino, A, Longobardi, G, Furgi, G, Rossi, M, Zoccolillo, N, Ferrara, N, Rengo, F: Left ventricular diastolic filling in diabetes mellitus with and without hypertension. Am J Hypertens 8:382–389, 1995PubMedGoogle Scholar
  62. 62.
    Redfield, MM, Jacobsen, SJ, Burnett, JC, Jr., Mahoney, DW, Bailey, KR, Rodeheffer, RJ: Burden of systolic and diastolic ventricular dysfunction in the community: appreciating the scope of the heart failure epidemic. JAMA 289:194–202, 2003PubMedGoogle Scholar
  63. 63.
    Poirier, P, Bogaty, P, Garneau, C, Marois, L, Dumesnil, JG: Diastolic dysfunction in normotensive men with well-controlled type 2 diabetes: importance of maneuvers in echocardiographic screening for preclinical diabetic cardiomyopathy. Diabetes Care 24:5–10, 2001PubMedGoogle Scholar
  64. 64.
    Bell, DS: Diabetic cardiomyopathy. Diabetes Care 26:2949–2951, 2003PubMedGoogle Scholar
  65. 65.
    Bell, DS: Diabetic cardiomyopathy. A unique entity or a complication of coronary artery disease? Diabetes Care 18:708–714, 1995PubMedGoogle Scholar
  66. 66.
    Trost, S, LeWinter, M: Diabetic cardiomyopathy. Curr Treat Options Cardiovasc Med 3:481–492, 2001PubMedGoogle Scholar
  67. 67.
    Salmasi, AM, Rawlins, S, Dancy, M: Left ventricular hypertrophy and preclinical impaired glucose tolerance and diabetes mellitus contribute to abnormal left ventricular diastolic function in hypertensive patients. Blood Press Monit 10:231–238, 2005PubMedGoogle Scholar
  68. 68.
    Saraiva, RM, Duarte, DM, Duarte, MP, Martins, AF, Poltronieri, AV, Ferreira, ME, Silva, MC, Hohleuwerger, R, Ellis, A, Rachid, MB, Monteiro, CF, Kaiser, SE: Tissue Doppler imaging identifies asymptomatic normotensive diabetics with diastolic dysfunction and reduced exercise tolerance. Echocardiography 22:561–570, 2005PubMedGoogle Scholar
  69. 69.
    Irace, L, Iarussi, D, Guadagno, I, De Rimini, ML, Lucca, P, Spadaro, P, Romano, A, Mansi, L, Iacono, A: Left ventricular function and exercise tolerance in patients with type II diabetes mellitus. Clin Cardiol 21:567–571, 1998PubMedGoogle Scholar
  70. 70.
    Fang, ZY, Sharman, J, Prins, JB, Marwick, TH: Determinants of exercise capacity in patients with type 2 diabetes. Diabetes Care 28:1643–1648, 2005PubMedGoogle Scholar
  71. 71.
    Sasso, FC, Carbonara, O, Cozzolino, D, Rambaldi, P, Mansi, L, Torella, D, Gentile, S, Turco, S, Torella, R, Salvatore, T: Effects of insulin-glucose infusion on left ventricular function at rest and during dynamic exercise in healthy subjects and noninsulin dependent diabetic patients: a radionuclide ventriculographic study. J Am Coll Cardiol 36:219–226, 2000PubMedGoogle Scholar
  72. 72.
    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 88:116–126, 1993PubMedGoogle Scholar
  73. 73.
    Belardinelli, R, Georgiou, D, Cianci, G, Berman, N, Ginzton, L, Purcaro, A: Exercise training improves left ventricular diastolic filling in patients with dilated cardiomyopathy. Clinical and prognostic implications. Circulation 91:2775–2784, 1995PubMedGoogle Scholar
  74. 74.
    Guazzi, M, Brambilla, R, Pontone, G, Agostoni, P, Guazzi, MD: Effect of non-insulin-dependent diabetes mellitus on pulmonary function and exercise tolerance in chronic congestive heart failure. Am J Cardiol 89:191–197, 2002PubMedGoogle Scholar
  75. 75.
    Tibb, AS, Ennezat, PV, Chen, JA, Haider, A, Gundewar, S, Cotarlan, V, Aggarwal, VS, Talreja, A, Le Jemtel, TH: Diabetes lowers aerobic capacity in heart failure. J Am Coll Cardiol 46:930–931, 2005PubMedGoogle Scholar
  76. 76.
    Ingle, L, Reddy, P, Clark, AL, Cleland, JG: Diabetes lowers six-minute walk test performance in heart failure. J Am Coll Cardiol 47:1909–1910, 2006PubMedGoogle Scholar
  77. 77.
    Lee, JC, Downing, SE: Effects of insulin on cardiac muscle contraction and responsiveness to norepinephrine. Am J Physiol 230:1360–1365, 1976PubMedGoogle Scholar
  78. 78.
    Downing, SE, Lee, JC: Myocardial and coronary vascular responses to insulin in the diabetic lamb. Am J Physiol 237:H514–H519, 1979PubMedGoogle Scholar
  79. 79.
    Fisher, BM, Gillen, G, Dargie, HJ, Inglis, GC, Frier, BM: The effects of insulin-induced hypoglycaemia on cardiovascular function in normal man: studies using radionuclide ventriculography. Diabetologia 30:841–845, 1987PubMedGoogle Scholar
  80. 80.
    Guazzi, M, Tumminello, G, Matturri, M, Guazzi, MD: Insulin ameliorates exercise ventilatory efficiency and oxygen uptake in patients with heart failure-type 2 diabetes comorbidity. J Am Coll Cardiol 42:1044–1050, 2003PubMedGoogle Scholar
  81. 81.
    McGavock, JM, Eves, ND, Mandic, S, Glenn, NM, Quinney, HA, Haykowsky, MJ: The role of exercise in the treatment of cardiovascular disease associated with type 2 diabetes mellitus. Sports Med 34:27–48, 2004PubMedGoogle Scholar
  82. 82.
    Stamler, J, Vaccaro, O, Neaton, JD, Wentworth, D: Diabetes, other risk factors, and 12-yr cardiovascular mortality for men screened in the Multiple Risk Factor Intervention Trial. Diabetes Care 16:434–444, 1993PubMedGoogle Scholar
  83. 83.
    Garcia, MJ, McNamara, PM, Gordon, T, Kannel, WB: Morbidity and mortality in diabetics in the Framingham population. Sixteen year follow-up study. Diabetes 23:105–111, 1974PubMedGoogle Scholar
  84. 84.
    Rytter, L, Troelsen, S, Beck-Nielsen, H: Prevalence and mortality of acute myocardial infarction in patients with diabetes. Diabetes Care 8:230–234, 1985PubMedGoogle Scholar
  85. 85.
    Granger, CB, Califf, RM, Young, S, Candela, R, Samaha, J, Worley, S, Kereiakes, DJ, Topol, EJ: Outcome of patients with diabetes mellitus and acute myocardial infarction treated with thrombolytic agents. The Thrombolysis and Angioplasty in Myocardial Infarction (TAMI) Study Group. J Am Coll Cardiol 21:920–925, 1993PubMedGoogle Scholar
  86. 86.
    Kavanagh, T, Mertens, DJ, Hamm, LF, Beyene, J, Kennedy, J, Corey, P, Shephard, RJ: Prediction of long-term prognosis in 12 169 men referred for cardiac rehabilitation. Circulation 106:666–671, 2002PubMedGoogle Scholar
  87. 87.
    Vanhees, L, Fagard, R, Thijs, L, Amery, A: Prognostic value of training-induced change in peak exercise capacity in patients with myocardial infarcts and patients with coronary bypass surgery. Am J Cardiol 76:1014–1019, 1995PubMedGoogle Scholar
  88. 88.
    Izawa, K, Tanabe, K, Omiya, K, Yamada, S, Yokoyama, Y, Ishiguro, T, Yagi, M, Hirano, Y, Kasahara, Y, Osada, N, Miyake, F, Murayama, M: Impaired chronotropic response to exercise in acute myocardial infarction patients with type 2 diabetes mellitus. Jpn Heart J 44:187–199, 2003PubMedGoogle Scholar
  89. 89.
    Verges, B, Patois-Verges, B, Cohen, M, Lucas, B, Galland-Jos, C, Casillas, JM: Effects of cardiac rehabilitation on exercise capacity in type 2 diabetic patients with coronary artery disease. Diabet Med 21:889–895, 2004PubMedGoogle Scholar
  90. 90.
    Colucci, WS, Ribeiro, JP, Rocco, MB, Quigg, RJ, Creager, MA, Marsh, JD, Gauthier, DF, Hartley, LH: Impaired chronotropic response to exercise in patients with congestive heart failure. Role of postsynaptic beta-adrenergic desensitization. Circulation 80:314–323, 1989PubMedGoogle Scholar
  91. 91.
    Endo, A, Kinugawa, T, Ogino, K, Kato, M, Hamada, T, Osaki, S, Igawa, O, Hisatome, I: Cardiac and plasma catecholamine responses to exercise in patients with type 2 diabetes: prognostic implications for cardiac-cerebrovascular events. Am J Med Sci 320:24–30, 2000PubMedGoogle Scholar
  92. 92.
    Oldridge, NB, Guyatt, GH, Fischer, ME, Rimm, AA: Cardiac rehabilitation after myocardial infarction. Combined experience of randomized clinical trials. JAMA 260:945–950, 1988PubMedGoogle Scholar
  93. 93.
    O'Connor, GT, Buring, JE, Yusuf, S, Goldhaber, SZ, Olmstead, EM, Paffenbarger, RS, Jr., Hennekens, CH: An overview of randomized trials of rehabilitation with exercise after myocardial infarction. Circulation 80:234–244, 1989PubMedGoogle Scholar
  94. 94.
    Dolan, NC, Liu, K, Criqui, MH, Greenland, P, Guralnik, JM, Chan, C, Schneider, JR, Mandapat, AL, Martin, G, McDermott, MM: Peripheral artery disease, diabetes, and reduced lower extremity functioning. Diabetes Care 25:113–120, 2002PubMedGoogle Scholar
  95. 95.
    Oka, RK, Sanders, MG: The impact of type 2 diabetes and peripheral arterial disease on quality of life. J Vasc Nurs 23:61–66, 2005PubMedGoogle Scholar
  96. 96.
    Katzel, LI, Sorkin, JD, Powell, CC, Gardner, AW: Comorbidities and exercise capacity in older patients with intermittent claudication. Vasc Med 6:157–162, 2001PubMedGoogle Scholar
  97. 97.
    Green, S, Askew, CD, Walker, PJ: Effect of type 2 diabetes mellitus on exercise intolerance and the physiological responses to exercise in peripheral arterial disease. Diabetologia 50:859–866, 2007PubMedGoogle Scholar
  98. 98.
    Gardner, AW, Poehlman, ET: Exercise rehabilitation programs for the treatment of claudication pain. A meta-analysis. JAMA 274:975–980, 1995PubMedGoogle Scholar
  99. 99.
    Sanderson, B, Askew, C, Stewart, I, Walker, P, Gibbs, H, Green, S: Short-term effects of cycle and treadmill training on exercise tolerance in peripheral arterial disease. J Vasc Surg 44:119–127, 2006PubMedGoogle Scholar
  100. 100.
    Ekroth, R, Dahllof, AG, Gundevall, B, Holm, J, Schersten, T: Physical training of patients with intermittent claudication: indications, methods, and results. Surgery 84:640–643, 1978PubMedGoogle Scholar
  101. 101.
    Liu, JE, Robbins, DC, Palmieri, V, Bella, JN, Roman, MJ, Fabsitz, R, Howard, BV, Welty, TK, Lee, ET, Devereux, RB: Association of albuminuria with systolic and diastolic left ventricular dysfunction in type 2 diabetes: the Strong Heart Study. J Am Coll Cardiol 41:2022–2028, 2003PubMedGoogle Scholar
  102. 102.
    Jensen, T, Richter, EA, Feldt-Rasmussen, B, Kelbaek, H, Deckert, T: Impaired aerobic work capacity in insulin dependent diabetics with increased urinary albumin excretion. Br Med J (Clin Res Ed) 296:1352–1354, 1988Google Scholar
  103. 103.
    Kelbaek, H, Jensen, T, Feldt-Rasmussen, B, Christensen, NJ, Richter, EA, Deckert, T, Nielsen, SL: Impaired left-ventricular function in insulin-dependent diabetic patients with increased urinary albumin excretion. Scand J Clin Lab Invest 51:467–473, 1991PubMedGoogle Scholar
  104. 104.
    Lau, AC, Lo, MK, Leung, GT, Choi, FP, Yam, LY, Wasserman, K: Altered exercise gas exchange as related to microalbuminuria in type 2 diabetic patients. Chest 125:1292–1298, 2004PubMedGoogle Scholar
  105. 105.
    Zoccali, C, Mallamaci, F, Tripepi, G: Traditional and emerging cardiovascular risk factors in end-stage renal disease. Kidney Int Suppl 63:S105–S110, 2003Google Scholar
  106. 106.
    Johansen, KL: Physical functioning and exercise capacity in patients on dialysis. Adv Ren Replace Ther 6:141–148, 1999PubMedGoogle Scholar
  107. 107.
    Painter, P, Messer-Rehak, D, Hanson, P, Zimmerman, SW, Glass, NR: Exercise capacity in hemodialysis, CAPD, and renal transplant patients. Nephron 42:47–51, 1986PubMedGoogle Scholar
  108. 108.
    Moore, GE, Brinker, KR, Stray-Gundersen, J, Mitchell, JH: Determinants of VO2peak in patients with end-stage renal disease: on and off dialysis. Med Sci Sports Exerc 25:18–23, 1993PubMedGoogle Scholar
  109. 109.
    Mayer, G, Thum, J, Cada, EM, Stummvoll, HK, Graf, H: Working capacity is increased following recombinant human erythropoietin treatment. Kidney Int 34:525–528, 1988PubMedGoogle Scholar
  110. 110.
    Painter, P, Moore, G, Carlson, L, Paul, S, Myll, J, Phillips, W, Haskell, W: Effects of exercise training plus normalization of hematocrit on exercise capacity and health-related quality of life. Am J Kidney Dis 39:257–265, 2002PubMedGoogle Scholar
  111. 111.
    Chan, CT, Notarius, CF, Merlocco, AC, Floras, JS: Improvement in exercise duration and capacity after conversion to nocturnal home haemodialysis. Nephrol Dial Transplant 22:3285–3291, 2007PubMedGoogle Scholar
  112. 112.
    Painter, P, Hanson, P, Messer-Rehak, D, Zimmerman, SW, Glass, NR: Exercise tolerance changes following renal transplantation. Am J Kidney Dis 10:452–456, 1987PubMedGoogle Scholar
  113. 113.
    Sigal, RJ, Kenny, GP, Wasserman, DH, Castaneda-Sceppa, C: Physical activity/exercise and type 2 diabetes. Diabetes Care 27:2518–2539, 2004PubMedGoogle Scholar
  114. 114.
    Sigal, RJ, Kenny, GP, Wasserman, DH, Castaneda-Sceppa, C, White, RD: Physical activity/exercise and type 2 diabetes: a consensus statement from the American Diabetes Association. Diabetes Care 29:1433–1438, 2006PubMedGoogle Scholar
  115. 115.
    Mogensen, CE: Nephropathy: early. In Handbook of Exercise in Diabetes. 2nd ed. Ruderman N, Devlin JT, Schneider SH, Kriska A, Eds. Alexandria, VA, American Diabetes Association, 2002, pp. 433–449Google Scholar
  116. 116.
    Romanelli, G, Giustina, A, Cravarezza, P, Caldonazzo, A, Agabiti-Rosei, E, Giustina, G: Albuminuria induced by exercise in hypertensive type I and type II diabetic patients: a randomised, double-blind study on the effects of acute administration of captopril and nifedipine. J Hum Hypertens 5:167–173, 1991PubMedGoogle Scholar
  117. 117.
    Hoogenberg, K, Dullaart, RP: Abnormal plasma noradrenaline response and exercise induced albuminuria in type 1 (insulin-dependent) diabetes mellitus. Scand J Clin Lab Invest 52:803–811, 1992PubMedGoogle Scholar
  118. 118.
    Viberti, GC, Jarrett, RJ, McCartney, M, Keen, H: Increased glomerular permeability to albumin induced by exercise in diabetic subjects. Diabetologia 14:293–300, 1978PubMedGoogle Scholar
  119. 119.
    Tuominen, JA, Ebeling, P, Koivisto, VA: Long-term lisinopril therapy reduces exercise-induced albuminuria in normoalbuminuric normotensive IDDM patients. Diabetes Care 21:1345–1348, 1998PubMedGoogle Scholar
  120. 120.
    Poulsen, PL, Ebbehoj, E, Mogensen, CE: Lisinopril reduces albuminuria during exercise in low grade microalbuminuric type 1 diabetic patients: a double blind randomized study. J Intern Med 249:433–440, 2001PubMedGoogle Scholar
  121. 121.
    Lane, JT, Ford, TC, Larson, LR, Chambers, WA, Lane, PH: Acute effects of different intensities of exercise in normoalbuminuric/normotensive patients with type 1 diabetes. Diabetes Care 27:28–32, 2004PubMedGoogle Scholar
  122. 122.
    Huttunen, NP, Kaar, M, Puukka, R, Akerblom, HK: Exercise-induced proteinuria in children and adolescents with type 1 (insulin dependent) diabetes. Diabetologia 21:495–497, 1981PubMedGoogle Scholar
  123. 123.
    Ward, KM, Mahan, JD, Sherman, WM: Aerobic training and diabetic nephropathy in the obese Zucker rat. Ann Clin Lab Sci 24:266–277, 1994PubMedGoogle Scholar
  124. 124.
    Albright, AL, Mahan, JD, Ward, KM, Sherman, WM, Roehrig, KL, Kirby, TE: Diabetic nephropathy in an aerobically trained rat model of diabetes. Med Sci Sports Exerc 27:1270–1277, 1995PubMedGoogle Scholar
  125. 125.
    Davison, SN: Pain in hemodialysis patients: prevalence, cause, severity, and management. Am J Kidney Dis 42:1239–1247, 2003PubMedGoogle Scholar
  126. 126.
    Parving, HH, Hommel, E, Mathiesen, E, Skott, P, Edsberg, B, Bahnsen, M, Lauritzen, M, Hougaard, P, Lauritzen, E: Prevalence of microalbuminuria, arterial hypertension, retinopathy and neuropathy in patients with insulin dependent diabetes. Br Med J (Clin Res Ed) 296:156–160, 1988Google Scholar
  127. 127.
    Cohen, JA, Jeffers, BW, Faldut, D, Marcoux, M, Schrier, RW: Risks for sensorimotor peripheral neuropathy and autonomic neuropathy in non-insulin-dependent diabetes mellitus (NIDDM). Muscle Nerve 21:72–80, 1998PubMedGoogle Scholar
  128. 128.
    Kay, J, Bardin, T: Osteoarticular disorders of renal origin: disease-related and iatrogenic. Baillieres Best Pract Res Clin Rheumatol 14:285–305, 2000PubMedGoogle Scholar
  129. 129.
    Kart-Koseoglu, H, Yucel, AE, Niron, EA, Koseoglu, H, Isiklar, I, Ozdemir, FN: Osteoarthritis in hemodialysis patients: relationships with bone mineral density and other clinical and laboratory parameters. Rheumatol Int 25:270–275, 2005PubMedGoogle Scholar
  130. 130.
    Naidich, JB, Mossey, RT, McHeffey-Atkinson, B, Karmel, MI, Bluestone, PA, Mailloux, LU, Stein, HL: Spondyloarthropathy from long-term hemodialysis. Radiology 167:761–764, 1988PubMedGoogle Scholar
  131. 131.
    Evans, N, Forsyth, E: End-stage renal disease in people with type 2 diabetes: systemic manifestations and exercise implications. Phys Ther 84:454–463, 2004PubMedGoogle Scholar
  132. 132.
    Kannel, WB, Abbott, RD, Savage, DD, McNamara, PM: Epidemiologic features of chronic atrial fibrillation: the Framingham study. N Engl J Med 306:1018–1022, 1982PubMedGoogle Scholar
  133. 133.
    Strongin, LG, Korneva, KG, Panova, EI: Disturbances of cardiac rhythm and metabolic control in patients with type-2 diabetes. Kardiologiia 45:46–49, 2005PubMedGoogle Scholar
  134. 134.
    Douketis, JD, Arneklev, K, Goldhaber, SZ, Spandorfer, J, Halperin, F, Horrow, J: Comparison of bleeding in patients with nonvalvular atrial fibrillation treated with ximelagatran or warfarin: assessment of incidence, case-fatality rate, time course and sites of bleeding, and risk factors for bleeding. Arch Intern Med 166:853–859, 2006PubMedGoogle Scholar
  135. 135.
    Haffner, SM, Lehto, S, Ronnemaa, T, Pyorala, K, Laakso, M: Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N Engl J Med 339:229–234, 1998PubMedGoogle Scholar
  136. 136.
    Kannel, WB, McGee, DL: Diabetes and cardiovascular risk factors: the Framingham study. Circulation 59:8–13, 1979PubMedGoogle Scholar
  137. 137.
    Guazzi, M, Belletti, S, Bianco, E, Lenatti, L, Guazzi, MD: Endothelial dysfunction and exercise performance in lone atrial fibrillation or associated with hypertension or diabetes: different results with cardioversion. Am J Physiol Heart Circ Physiol 291:H921–H928, 2006PubMedGoogle Scholar
  138. 138.
    Wei, M, Gibbons, LW, Kampert, JB, Nichaman, MZ, Blair, SN: Low cardiorespiratory fitness and physical inactivity as predictors of mortality in men with type 2 diabetes. Ann Intern Med 132:605–611, 2000PubMedGoogle Scholar

Copyright information

© Humana Press, a part of Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Amy G. Huebschmann
    • 1
  • Judith G. Regensteiner
    • 2
  1. 1.Division of General Internal Medicine, Department of MedicineUniversity of Colorado DenverAuroraUSA
  2. 2.Divisions of General Internal Medicine and CardiologyDepartment of Medicine, University of Colorado DenverAuroraUSA

Personalised recommendations