Table of Contents Author Guidelines Submit a Manuscript
Journal of Diabetes Research
Volume 2015 (2015), Article ID 654204, 11 pages
http://dx.doi.org/10.1155/2015/654204
Review Article

Cardiovascular Control during Exercise in Type 2 Diabetes Mellitus

1School of Science and Health, University of Western Sydney, Sydney, NSW 2751, Australia
2Neuroscience Research Australia, Sydney, NSW 2751, Australia
3Department of Physiology, School of Medicine, Trinity College Dublin, Dublin 1, Ireland
4Department of Medicine, University of Otago, Dunedin, Otago 9054, New Zealand
5Department of Physiology-HeartOtago, University of Otago, Dunedin, Otago 9054, New Zealand
6Division of General Internal Medicine, Center for Women’s Health Research, Department of Medicine, School of Medicine, University of Colorado, Denver, CO 80210, USA

Received 22 January 2015; Accepted 17 March 2015

Academic Editor: Raffaele Marfella

Copyright © 2015 Simon Green et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. G. Regensteiner, “Type 2 diabetes mellitus and cardiovascular exercise performance,” Reviews in Endocrine and Metabolic Disorders, vol. 5, no. 3, pp. 269–276, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. J. E. B. Reusch, M. Bridenstine, and J. G. Regensteiner, “Type 2 diabetes mellitus and exercise impairment,” Reviews in Endocrine and Metabolic Disorders, vol. 14, no. 1, pp. 77–86, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. J. R. Levick, An Introduction to Cardiovascular Physiology, Arnold Publishers, London, UK, 4th edition, 2003.
  4. R. M. Berne and M. N. Levy, Cardiovascular Physiology, Mosby, St. Louis, Mo, USA, 8th edition, 2001.
  5. J. V. Tyberg, “How changes in venous capacitance modulate cardiac output,” Pflügers Archiv, vol. 445, no. 1, pp. 10–17, 2002. View at Publisher · View at Google Scholar · View at Scopus
  6. L. B. Rowell, Human Cardiovascular Control, Oxford University Press, New York, NY, USA, 1993.
  7. R. L. H. Sprangers, K. H. Wesseling, A. L. T. Imholz, B. P. M. Impholz, and W. Wieling, “Initial blood pressure fall on stand up and exercise explained by changes in total peripheral resistance,” Journal of Applied Physiology, vol. 70, no. 2, pp. 523–530, 1991. View at Publisher · View at Google Scholar · View at Scopus
  8. W. Wieling, M. P. M. Harms, A. D. J. Ten Harkel, J. J. Van Lieshout, and R. L. H. Sprangers, “Circulatory response evoked by a 3 s bout of dynamic leg exercise in humans,” The Journal of Physiology, vol. 494, no. 2, pp. 601–611, 1996. View at Publisher · View at Google Scholar · View at Scopus
  9. J. A. Dempsey, M. Amann, L. M. Romer, and J. D. Miller, “Respiratory system determinants of peripheral fatigue and endurance performance,” Medicine and Science in Sports and Exercise, vol. 40, no. 3, pp. 457–461, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. J. González-Alonso, J. A. L. Calbet, and B. Nielsen, “Muscle blood flow is reduced with dehydration during prolonged exercise in humans,” The Journal of Physiology, vol. 513, no. 3, pp. 895–905, 1998. View at Publisher · View at Google Scholar · View at Scopus
  11. E. O'Connor, S. Green, C. Kiely, D. O'Shea, and M. Egaña, “Differential effects of age and type 2 diabetes on dynamic versus peak response of pulmonary oxygen uptake during exercise,” Journal of Applied Physiology, 2015. View at Publisher · View at Google Scholar
  12. J. G. Regensteiner, T. A. Bauer, J. E. B. Reusch et al., “Cardiac dysfunction during exercise in uncomplicated type 2 diabetes,” Medicine & Science in Sports & Exercise, vol. 41, no. 5, pp. 977–984, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. J. A. Scott, J. S. Coombes, J. B. Prins, R. L. Leano, T. H. Marwick, and J. E. Sharman, “Patients with type 2 diabetes have exaggerated brachial and central exercise blood pressure: relation to left ventricular relative wall thickness,” American Journal of Hypertension, vol. 21, no. 6, pp. 715–721, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. T. E. Pinto, S. Gusso, P. L. Hofman et al., “Systolic and diastolic abnormalities reduce the cardiac response to exercise in adolescents with type 2 diabetes,” Diabetes Care, vol. 37, no. 5, pp. 1439–1446, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. J. C. Baldi, J. L. Aoina, H. C. Oxenham, W. Bagg, and R. N. Doughty, “Reduced exercise arteriovenous O2 difference in Type 2 diabetes,” Journal of Applied Physiology, vol. 94, no. 3, pp. 1033–1038, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. T. M. Roy, H. R. Petterson, H. L. Snider et al., “Autonomic influence on cardiovascular performance in diabetic subjects,” The American Journal of Medicine, vol. 87, no. 4, pp. 382–388, 1989. View at Publisher · View at Google Scholar · View at Scopus
  17. J. G. Regensteiner, T. A. Bauer, A. G. Huebschmann et al., “Sex differences in the effects of type 2 diabetes on exercise performance,” Medicine & Science in Sports & Exercise, vol. 47, no. 1, pp. 58–65, 2015. View at Publisher · View at Google Scholar · View at Scopus
  18. J. G. Regensteiner, T. A. Bauer, J. E. B. Reusch et al., “Abnormal oxygen uptake kinetic responses in women with type II diabetes mellitus,” Journal of Applied Physiology, vol. 85, no. 1, pp. 310–317, 1998. View at Google Scholar · View at Scopus
  19. O. MacAnaney, J. Malone, S. Warmington, D. O’Shea, S. Green, and M. Egana, “Cardiac output responses are not related to the slowed oxygen uptake kinetics in type 2 diabetes,” Medicine and Science in Sports and Exercise, vol. 43, no. 6, pp. 935–942, 2011. View at Google Scholar
  20. E. O’Connor, C. Kiely, D. O’Shea, S. Green, and M. Egana, “Similar level of impairment in exercise tolerance and VO2 kinetics in middle aged men and women,” American Journal of Physiology—Regulatory and Integrative Physiology, vol. 303, pp. R70–R76, 2012. View at Google Scholar
  21. S. Lalande, S. Gusso, P. L. Hofman, and J. C. Baldi, “Reduced leg blood flow during submaximal exercise in type 2 diabetes,” Medicine & Science in Sports & Exercise, vol. 40, no. 4, pp. 612–617, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. J. G. Regensteiner, J. Sippel, E. T. McFarling, E. E. Wolfel, and W. R. Hiatt, “Effects of non-insulin dependent diabetes on oxygen consumption during treadmill exercise,” Medicine & Science in Sports & Exercise, vol. 27, no. 5, pp. 661–667, 1995. View at Google Scholar · View at Scopus
  23. D. P. Wilkerson, D. C. Poole, A. M. Jones et al., “Older type 2 diabetic males do not exhibit abnormal pulmonary oxygen uptake and muscle oxygen utilization dynamics during submaximal cycling exercise,” American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 300, no. 3, pp. R685–R692, 2011. View at Publisher · View at Google Scholar · View at Scopus
  24. S. L. Brandenburg, J. E. B. Reusch, T. A. Bauer, B. W. Jeffers, W. R. Hiatt, and J. G. Regensteiner, “Effects of exercise training on oxygen uptake kinetic responses in women with type 2 diabetes,” Diabetes Care, vol. 22, no. 10, pp. 1640–1646, 1999. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Gusso, P. Hofman, S. Lalande, W. Cutfield, E. Robinson, and J. C. Baldi, “Impaired stroke volume and aerobic capacity in female adolescents with type 1 and type 2 diabetes mellitus,” Diabetologia, vol. 51, no. 7, pp. 1317–1320, 2008. View at Publisher · View at Google Scholar · View at Scopus
  26. J. C. Baldi, J. L. Aoina, G. A. Whalley et al., “The effect of type 2 diabetes on diastolic function,” Medicine and Science in Sports and Exercise, vol. 38, no. 8, pp. 1384–1388, 2006. View at Publisher · View at Google Scholar · View at Scopus
  27. S. Lalande, P. L. Hofman, and J. C. Baldi, “Effect of reduced total blood volume on left ventricular volumes and kinetics in type 2 diabetes,” Acta Physiologica, vol. 199, no. 1, pp. 23–30, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. C. Kiely, E. O’Connor, D. O’Shea, S. Green, and M. Egana, “Hemodynamic responses during graded and constant-load plantar flexion exercise in middle-aged men and women with type 2 diabetes,” Journal of Applied Physiology, vol. 117, no. 7, pp. 755–764, 2014. View at Publisher · View at Google Scholar
  29. B. A. Kingwell, M. Formosa, M. Muhlmann, S. J. Bradley, and G. K. McConell, “Type 2 diabetic individuals have impaired leg blood flow responses to exercise: role of endothelium-dependent vasodilation,” Diabetes Care, vol. 26, no. 3, pp. 899–904, 2003. View at Publisher · View at Google Scholar · View at Scopus
  30. B. A. Kingwell, M. Formosa, M. Muhlmann, S. J. Bradley, and G. K. McConell, “Nitric oxide synthase inhibition reduces glucose uptake during exercise in individuals with type 2 diabetes more than in control subjects,” Diabetes, vol. 51, no. 8, pp. 2572–2580, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. O. MacAnaney, H. Reilly, D. O’Shea, M. Egaña, and S. Green, “Effect of type 2 diabetes on the dynamic response characteristics of leg vascular conductance during exercise,” Diabetes and Vascular Disease Research, vol. 8, no. 1, pp. 12–21, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. I. K. Martin, A. Katz, and J. Wahren, “Splanchnic and muscle metabolism during exercise in NIDDM patients,” The American Journal of Physiology—Endocrinology and Metabolism, vol. 269, no. 3, pp. E583–E590, 1995. View at Google Scholar · View at Scopus
  33. M. Egaña and S. Green, “Effect of body tilt on calf muscle performance and blood flow in humans,” Journal of Applied Physiology, vol. 98, no. 6, pp. 2249–2258, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Green, R. Thorp, E. J. Reeder, J. Donnelly, and G. Fordy, “Venous occlusion plethysmography versus doppler ultrasound in the assessment of leg blood flow during calf exercise,” European Journal of Applied Physiology, vol. 111, no. 8, pp. 1889–1900, 2011. View at Publisher · View at Google Scholar · View at Scopus
  35. E. J. Reeder and S. Green, “Dynamic response characteristics of hyperaemia in the human calf muscle: effect of exercise intensity and relation to electromyographic activity,” European Journal of Applied Physiology, vol. 112, no. 12, pp. 3997–4013, 2012. View at Publisher · View at Google Scholar · View at Scopus
  36. B. Grassi, D. C. Poole, R. S. Richardson, D. R. Knight, B. K. Erickson, and P. D. Wagner, “Muscle O2 uptake kinetics in humans: implications for metabolic control,” Journal of Applied Physiology, vol. 80, no. 3, pp. 988–998, 1996. View at Google Scholar · View at Scopus
  37. N. R. Saunders, K. E. Pyke, and M. E. Tschakovsky, “Dynamic response characteristics of local muscle blood flow regulatory mechanisms in human forearm exercise,” Journal of Applied Physiology, vol. 98, no. 4, pp. 1286–1296, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. J. Donnelly and S. Green, “Effect of hypoxia on the dynamic response of hyperaemia in the contracting human calf muscle,” Experimental Physiology, vol. 98, no. 1, pp. 81–93, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. W. Bakker, E. C. Eringa, P. Sipkema, and V. W. M. Van Hinsbergh, “Endothelial dysfunction and diabetes: Roles of hyperglycemia, impaired insulin signaling and obesity,” Cell and Tissue Research, vol. 335, no. 1, pp. 165–189, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. E. J. Barrett and S. Rattigan, “Muscle perfusion: its measurement and role in metabolic regulation,” Diabetes, vol. 61, no. 11, pp. 2661–2668, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. M. A. Delbin and A. J. Trask, “The diabetic vasculature: physiological mechanisms of dysfunction and influence of aerobic exercise training in animal models,” Life Sciences, vol. 102, no. 1, pp. 1–9, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Avogaro, M. Albiero, L. Menegazzo, S. de Kreutzenberg, and G. P. Fadini, “Endothelial dysfunction in diabetes: the role of reparatory mechanisms,” Diabetes Care, vol. 34, supplement 2, pp. S285–S290, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. G. E. McVeigh, G. M. Brennan, G. D. Johnston et al., “Impaired endothelium-dependent and independent vasodilation in patients with Type 2 (non-insulin-dependent) diabetes mellitus,” Diabetologia, vol. 35, no. 8, pp. 771–776, 1992. View at Google Scholar · View at Scopus
  44. L. A. Lesniewski, A. J. Donato, B. J. Behnke et al., “Decreased NO signaling leads to enhanced vasoconstrictor responsiveness in skeletal muscle arterioles of the ZDF rat prior to overt diabetes and hypertension,” American Journal of Physiology: Heart and Circulatory Physiology, vol. 294, no. 4, pp. H1840–H1850, 2008. View at Publisher · View at Google Scholar · View at Scopus
  45. N. M. Novielli, B. K. Al-Khazraji, P. J. Medeiros, D. Goldman, and D. N. Jackson, “Pre-diabetes augments neuropeptide Y(1)- and alpha(1)-receptor control of basal hindlimb vascular tone in young ZDF rats,” PLoS ONE, vol. 7, no. 10, Article ID e46659, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. N. M. Novielli and D. N. Jackson, “Contraction-evoked vasodilation and functional hyperaemia are compromised in branching skeletal muscle arterioles of young pre-diabetic mice,” Acta Physiologica, vol. 211, no. 2, pp. 371–384, 2014. View at Publisher · View at Google Scholar · View at Scopus
  47. S. J. Haug and S. S. Segal, “Sympathetic neural inhibition of conducted vasodilatation along hamster feed arteries: complementary effects of α1- and α2-adrenoreceptor activation,” The Journal of Physiology, vol. 563, no. 2, pp. 541–555, 2005. View at Publisher · View at Google Scholar · View at Scopus
  48. J. W. G. E. Van Teeffelen and S. S. Segal, “Interaction between sympathetic nerve activation and muscle fibre contraction in resistance vessels of hamster retractor muscle,” The Journal of Physiology, vol. 550, no. 2, pp. 563–574, 2003. View at Publisher · View at Google Scholar · View at Scopus
  49. W. L. Sexton, “Skeletal muscle vascular transport capacity in diabetic rats,” Diabetes, vol. 43, no. 2, pp. 225–231, 1994. View at Publisher · View at Google Scholar · View at Scopus
  50. D. C. Poole, “Role of exercising muscle in slow component of VO2,” Medicine and Science in Sports and Exercise, vol. 26, no. 11, pp. 1335–1340, 1994. View at Google Scholar · View at Scopus
  51. H. B. Rossiter, S. A. Ward, V. L. Doyle, F. A. Howe, J. R. Griffiths, and B. J. Whipp, “Inferences from pulmonary O2 uptake with respect to intramuscular [phosphocreatine] kinetics during moderate exercise in humans,” The Journal of Physiology, vol. 518, no. 3, pp. 921–932, 1999. View at Publisher · View at Google Scholar · View at Scopus
  52. B. J. Behnke, C. A. Kindig, P. McDonough, D. C. Poole, and W. L. Sexton, “Dynamics of microvascular oxygen pressure during rest-contraction transition in skeletal muscle of diabetic rats,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 283, no. 3, pp. H926–H932, 2002. View at Publisher · View at Google Scholar · View at Scopus
  53. R. Fitzpatrick, J. L. Taylor, and D. I. McCloskey, “Effects of arterial perfusion pressure on force production in working human hand muscles,” Journal of Physiology, vol. 495, no. 3, pp. 885–891, 1996. View at Publisher · View at Google Scholar · View at Scopus
  54. L. Hirvonen and R. R. Sonnenschein, “Relation between blood flow and contraction force in active skeletal muscle,” Circulation Research, vol. 10, pp. 94–104, 1962. View at Publisher · View at Google Scholar · View at Scopus
  55. S. F. Hobbs and D. I. McCloskey, “Effects of blood pressure on force production in cat and human muscle,” Journal of Applied Physiology, vol. 63, no. 2, pp. 834–839, 1987. View at Google Scholar · View at Scopus
  56. M. Egaña and S. Green, “Intensity-dependent effect of body tilt angle on calf muscle fatigue in humans,” European Journal of Applied Physiology, vol. 99, no. 1, pp. 1–9, 2007. View at Publisher · View at Google Scholar · View at Scopus
  57. M. J. Macdonald, J. K. Shoemaker, M. E. Tschakovsky, and R. L. Hughson, “Alveolar oxygen uptake and femoral artery blood flow dynamics in upright and supine leg exercise in humans,” Journal of Applied Physiology, vol. 85, no. 5, pp. 1622–1628, 1998. View at Google Scholar · View at Scopus
  58. M. Egaña, K. Ryan, S. A. Warmington, and S. Green, “Effect of body tilt angle on fatigue and EMG activities in lower limbs during cycling,” European Journal of Applied Physiology, vol. 108, no. 4, pp. 649–656, 2010. View at Publisher · View at Google Scholar · View at Scopus
  59. M. Egaña, S. Green, E. J. Garrigan, and S. Warmington, “Effect of posture on high-intensity constant-load cycling performance in men and women,” European Journal of Applied Physiology, vol. 96, no. 1, pp. 1–9, 2006. View at Publisher · View at Google Scholar · View at Scopus
  60. M. Egaña, S. Smith, and S. Green, “Revisiting the effect of posture on high-intensity constant-load cycling performance in men and women,” European Journal of Applied Physiology, vol. 99, no. 5, pp. 495–501, 2007. View at Publisher · View at Google Scholar · View at Scopus
  61. J. K. Limberg, B. J. Morgan, J. J. Sebranek, L. T. Proctor, M. W. Eldridge, and W. G. Schrage, “Neural control of blood flow during exercise in human metabolic syndrome,” Experimental Physiology, vol. 99, no. 9, pp. 1191–1202, 2014. View at Publisher · View at Google Scholar · View at Scopus
  62. S. Green and E. Cameron, “Interactive effect of acute sympathetic activation and exercise intensity on the dynamic response characteristics of vascular conductance in the human calf muscle,” European Journal of Applied Physiology, 2014. View at Publisher · View at Google Scholar