Impaired cerebral blood flow and oxygenation during exercise in type 2 diabetic patients

Physiological Reports

Volumn 3, Issue 6, 2015, Pages

  Kim, Yu Sok ^a   Seifert, Thomas ^b   Brassard, Patrice ^b,e   Rasmussen, Peter ^b   Vaag, Allan ^c   Nielsen, Henning B ^b   Secher, Niels H ^b   van Lieshout, Johannes J ^a,d  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF COPENHAGEN   (Denmark)

^c UNIVERSITY OF COPENHAGEN   (Denmark)

^d UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^e LAVAL UNIVERSITY   (Canada)

Author keywords

Cardiac output; Cerebral autoregulation; Cerebral circulation; Cerebral perfusion; Cerebrovascular conductance

Indexed keywords

GLUCOSE; LACTIC ACID; OXYGEN;

ADULT; ARTERIAL CARBON DIOXIDE TENSION; ARTERIAL OXYGEN TENSION; ARTICLE; AUTOREGULATION; BICYCLE ERGOMETER; BLOOD FLOW VELOCITY; BRAIN ISCHEMIA; BRAIN OXYGEN TENSION; BRAIN PERFUSION; CARDIOVASCULAR FUNCTION; CEREBRAL METABOLIC RATE OF OXYGEN; CEREBROVASCULAR AUTOREGULATION; CLINICAL ARTICLE; CONTROLLED STUDY; EXERCISE; HEART OUTPUT; HEART OUTPUT MEASUREMENT; HEMODYNAMICS; HUMAN; MALE; MIDDLE AGED; MIDDLE CEREBRAL ARTERY; NON INSULIN DEPENDENT DIABETES MELLITUS; OXYGEN SATURATION; OXYGENATION; TRANSCRANIAL DOPPLER ULTRASONOGRAPHY;

EID: 85005965323     PISSN: None     EISSN: 2051817X     Source Type: Journal    
DOI: 10.14814/phy2.12430     Document Type: Article

References (55)

1. Bada, A. A., J. H. Svendsen, N. H. Secher, B. Saltin, and S. P. Mortensen. 2012. Peripheral vasodilation determines cardiac output in exercising humans: insight from atrial pacing. J. Physiol. 590:2051–2060.
2. Bauer, T. A., J. E. Reusch, M. Levi, and J. G. Regensteiner. 2007. Skeletal muscle deoxygenation after the onset of moderate exercise suggests slowed microvascular blood flow kinetics in type 2 diabetes. Diabetes Care 30:2880–2885.
3. Borg, G. 1970. Perceived exertion as an indicator of somatic stress. Scand. J. Rehabil. Med. 2:92–98.
4. Brassard, P., S. Legault, C. Garneau, P. Bogaty, J. G. Dumesnil, and P. Poirier. 2007. Normalization of diastolic dysfunction in type 2 diabetics after exercise training. Med. Sci. Sports Exerc. 39:1896–1901.
5. Estacio, R. O., J. G. Regensteiner, E. E. Wolfel, B. Jeffers, M. Dickenson, and R. W. Schrier. 1998. The association between diabetic complications and exercise capacity in NIDDM patients. Diabetes Care 21:291–295.
6. Fang, Z. Y., J. Sharman, J. B. Prins, and T. H. Marwick. 2005. Determinants of exercise capacity in patients with type 2 diabetes. Diabetes Care 28:1643–1648.
7. Fisher, J. P., D. Hartwich, T. Seifert, N. D. Olesen, C. L. McNulty, H. B. Nielsen, et al. 2013. Cerebral perfusion, oxygenation and metabolism during exercise in young and elderly individuals. J. Physiol. 591:1859–1870.
8. Fluck, D., I. D. Braz, S. Keiser, F. Huppin, T. Haider, M. Hilty, et al. 2014. Age, aerobic fitness and cerebral perfusion during exercise: role of carbon dioxide. Am. J. Physiol. Heart Circ. Physiol. 307:H515–H523.
9. Fox, P. T., and M. E. Raichle. 1986. Focal physiological uncoupling of cerebral blood flow and oxidative metabolism during somatosensory stimulation in human subjects. Proc. Natl Acad. Sci. USA 83:1140–1144.
10. Gjedde, A., P. Johannsen, G. E. Cold, and L. Ostergaard. 2005. Cerebral metabolic response to low blood flow: possible role of cytochrome oxidase inhibition. J. Cereb. Blood Flow Metab. 25:1183–1196.
11. Gonzalez-Alonso, J., M. K. Dalsgaard, T. Osada, S. Volianitis, E. A. Dawson, C. C. Yoshiga, et al. 2004. Brain and central hemodynamics and oxygenation during maximal exercise in humans. J. Physiol. 557:331–342.
12. Goodall, S., R. Twomey, M. Amann, E. Z. Ross, A. T. Lovering, L. M. Romer, et al. 2014. AltitudeOmics: exerciseinduced supraspinal fatigue is attenuated in healthy humans after acclimatization to high altitude. Acta Physiol. 210:875–888.
13. Gruhn, N., F. S. Larsen, S. Boesgaard, G. M. Knudsen, S. A. Mortensen, G. Thomsen, et al. 2001. Cerebral blood flow in patients with chronic heart failure before and after heart transplantation. Stroke 32:2530–2533.
14. Hellstrõm, G., W. Fischer-Colbrie, N. G. Wahlgren, and T. Jøgestrand. 1996. Carotid artery blood flow and middle cerebral artery blood flow velocity during physical exercise. J. Appl. Physiol. 81:413–418.
15. Hirth, C., H. Obrig, J. Valdueza, U. Dirnagl, and A. Villringer. 1997. Simultaneous assessment of cerebral oxygenation and hemodynamics during a motor task. A combined near infrared and transcranial Doppler sonography study. Adv. Exp. Med. Biol. 411:461–469.
16. Ide, K., and N. H. Secher. 2000. Cerebral blood flow and metabolism during exercise. Prog. Neurobiol. 61:397–414.
17. Ide, K., F. Pott, J. J. Van Lieshout, and N. H. Secher. 1998. Middle cerebral artery blood velocity depends on cardiac output during exercise with a large muscle mass. Acta Physiol. Scand. 162:13–20.
18. Ide, K., A. L. Gullov, F. Pott, J. J. Van Lieshout, B. G. Koefoed, P. Petersen, et al. 1999a. Middle cerebral artery blood velocity during exercise in patients with atrial fibrillation. Clin. Physiol. 19:284–289.
19. Ide, K., A. Horn, and N. H. Secher. 1999b. Cerebral metabolic response to submaximal exercise. J. Appl. Physiol. 87: 1604–1608.
20. Immink, R. V., B. J. van den Born, G. A. van Montfrans, R. P. Koopmans, J. M. Karemaker, and J. J. van Lieshout. 2004. Impaired cerebral autoregulation in patients with malignant hypertension. Circulation 110:2241–2245.
21. Imray, C. H., S. D. Myers, K. T. Pattinson, A. R. Bradwell, C. W. Chan, S. Harris, et al. 2005. Effect of exercise on cerebral perfusion in humans at high altitude. J. Appl. Physiol. 99:699–706.
22. Jellema, W. T., K. H. Wesseling, A. B. Groeneveld, C. P. Stoutenbeek, L. G. Thijs, and J. J. van Lieshout. 1999. Continuous cardiac output in septic shock by simulating a model of the aortic input impedance: a comparison with bolus injection thermodilution. Anesthesiology 90:1317–1328.
23. Jorgensen, L. G., G. Perko, and N. H. Secher. 1992. Regional cerebral artery mean flow velocity and blood flow during dynamic exercise in humans. J. Appl. Physiol. 73: 1825–1830.
24. Kim, Y. S., R. Krogh-Madsen, P. Rasmussen, P. Plomgaard, S. Ogoh, N. H. Secher, et al. 2007. Effects of hyperglycemia on the cerebrovascular response to rhythmic handgrip exercise. Am. J. Physiol. Heart Circ. Physiol. 293:H467–H473.
25. Kim, Y. S., S. C. Davis, J. Truijen, W. J. Stok, N. H. Secher, and J. J. van Lieshout. 2011. Intensive blood pressure control affects cerebral blood flow in type 2 diabetes mellitus patients. Hypertension 57:738–745.
26. Kingwell, B. A., M. Formosa, M. Muhlmann, S. J. Bradley, and G. K. McConell. 2003. Type 2 diabetic individuals have impaired leg blood flow responses to exercise - Role of endothelium-dependent vasodilation. Diabetes Care 26:899–904.
27. Laughlin, M. H., M. J. Davis, N. H. Secher, J. J. van Lieshout, A. A. Arce-Esquivel, G. H. Simmons, et al. 2012. Peripheral circulation. Compr Physiol. 2:321–447.
28. Lavi, S., D. Gaitini, V. Milloul, and G. Jacob. 2006. Impaired cerebral CO2 vasoreactivity: association with endothelial dysfunction. Am. J. Physiol. Heart Circ. Physiol. 291: H1856–H1861.
29. Madsen, P. L., S. Holm, M. Herning, and N. A. Lassen. 1993. Average blood flow and oxygen uptake in the human brain during resting wakefulness: a critical appraisal of the Kety- Schmidt technique. J. Cereb. Blood Flow Metab. 13:646–655.
30. Mortensen, S. P., R. Damsgaard, E. A. Dawson, N. H. Secher, and J. Gonzalez-Alonso. 2008. Restrictions in systemic and locomotor skeletal muscle perfusion, oxygen supply and VO2 during high-intensity whole-body exercise in humans. J. Physiol. 586:2621–2635.
31. Nybo, L., and P. Rasmussen. 2007. Inadequate cerebral oxygen delivery and central fatigue during strenuous exercise. Exerc. Sport Sci. Rev. 35:110–118.
32. Obrig, H., C. Hirth, J. G. Junge-Hulsing, C. Doge, T. Wolf, U. Dirnagl, et al. 1996. Cerebral oxygenation changes in response to motor stimulation. J. Appl. Physiol. 81:1174–1183.
33. Ogoh, S., R. M. Brothers, Q. Barnes, W. L. Eubank, M. N. Hawkins, S. Purkayastha, et al. 2005. The effect of changes in cardiac output on middle cerebral artery mean blood velocity at rest and during exercise. J. Physiol. 569:697–704.
34. Palazzo, P., P. Maggio, R. Altavilla, A. Di Flaviani, I. Giordani, I. Malandrucco, et al. 2013. Cerebral hemodynamics and systemic endothelial function are already impaired in wellcontrolled type 2 diabetic patients, with short-term disease. PLoS ONE 8:e83287.
35. Phillips, B., J. Williams, P. Atherton, K. Smith, W. Hildebrandt, D. Rankin, et al. 2012. Resistance exercise training improves age-related declines in leg vascular conductance and rejuvenates acute leg blood flow responses to feeding and exercise. J. Appl. Physiol. 112:347–353.
36. Pinto, T. E., S. Gusso, P. L. Hofman, J. G. Derraik, T. S. Hornung, W. S. Cutfield, et al. 2014. Systolic and diastolic abnormalities reduce the cardiac response to exercise in adolescents with type 2 diabetes. Diabetes Care 37:1439–1446.
37. Poirier, P., C. Garneau, P. Bogaty, A. Nadeau, L. Marois, C. Brochu, et al. 2000. 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.
38. Rasmussen, P., E. A. Dawson, L. Nybo, J. J. van Lieshout, N. H. Secher, and A. Gjedde. 2007. Capillary-oxygenation-leveldependent near-infrared spectrometry in frontal lobe of humans. J. Cereb. Blood Flow Metab. 27:1082–1093.
39. Rasmussen, P., J. Nielsen, M. Overgaard, R. Krogh-Madsen, A. Gjedde, N. H. Secher, et al. 2010. Reduced muscle activation during exercise related to brain oxygenation and metabolism in humans. J. Physiol. 588:1985–1995.
40. Rasmussen, P., Y. S. Kim, R. Krogh-Madsen, C. Lundby, N. V. Olsen, N. H. Secher, et al. 2012. Both acute and prolonged administration of EPO reduce cerebral and systemic vascular conductance in humans. FASEB J. 26:1343–1348.
41. Regensteiner, J. G., T. A. Bauer, J. E. Reusch, R. A. Quaife, M. Y. Chen, S. C. Smith, et al. 2009. Cardiac dysfunction during exercise in uncomplicated type 2 diabetes. Med. Sci. Sports Exerc. 41:977–984.
42. Regensteiner, J. G., T. A. Bauer, A. G. Huebschmann, L. Herlache, H. D. Weinberger, E. E. Wolfel, et al. 2015. Sex Differences in the Effects of Type 2 Diabetes on Exercise Performance. Med. Sci. Sports Exerc. 47:58–65.
43. Ritz, K., N. P. Denswil, O. C. Stam, J. J. van Lieshout, and M. J. Daemen. 2014. Cause and mechanisms of intracranial atherosclerosis. Circulation 130:1407–1414.
44. Rupp, T., and S. Perrey. 2008. Prefrontal cortex oxygenation and neuromuscular responses to exhaustive exercise. Eur. J. Appl. Physiol. 102:153–163.
45. Scheuermann-Freestone, M., P. L. Madsen, D. Manners, A. M. Blamire, R. E. Buckingham, P. Styles, et al. 2003. Abnormal cardiac and skeletal muscle energy metabolism in patients with type 2 diabetes. Circulation 107:3040–3046.
46. Schofield, I., R. Malik, A. Izzard, C. Austin, and A. Heagerty. 2002. Vascular structural and functional changes in type 2 diabetes mellitus: evidence for the roles of abnormal myogenic responsiveness and dyslipidemia. Circulation 106:3037–3043.
47. Secher, N. H., T. Seifert, and J. J. Van Lieshout. 2008. Cerebral blood flow and metabolism during exercise: implications for fatigue. J. Appl. Physiol. 104:306–314.
48. Seifert, T., P. Rasmussen, N. H. Secher, and H. B. Nielsen. 2008. Cerebral oxygenation decreases during exercise in humans with beta-adrenergic blockade. Acta Physiol. 196:295–302.
49. Shaw, T. G., K. F. Mortel, J. S. Meyer, R. L. Rogers, J. Hardenberg, and M. M. Cutaia. 1984. Cerebral blood flow changes in benign aging and cerebrovascular disease. Neurology 34:855–862.
50. Subudhi, A. W., J. T. Olin, A. C. Dimmen, D. M. Polaner, B. Kayser, and R. C. Roach. 2011. Does cerebral oxygen delivery limit incremental exercise performance? J. Appl. Physiol. 111:1727–1734.
51. Taegtmeyer, H., P. McNulty, and M. E. Young. 2002. Adaptation and maladaptation of the heart in diabetes: Part I: general concepts. Circulation 105:1727–1733.
52. Thomas, S. N., T. Schroeder, N. H. Secher, and J. H. Mitchell. 1989. Cerebral blood flow during submaximal and maximal dynamic exercise in humans. J. Appl. Physiol. 67:744–748.
53. Van Lieshout, J. J., F. Pott, P. L. Madsen, J. van Goudoever, and N. H. Secher. 2001. Muscle tensing during standing: effects on cerebral tissue oxygenation and cerebral artery blood velocity. Stroke 32:1546–1551.
54. Verbree, J., A. S. Bronzwaer, E. Ghariq, M. J. Versluis, M. J. Daemen, M. A. van Buchem, et al. 2014. Assessment of middle cerebral artery diameter during hypocapnia and hypercapnia in humans using ultra-high-field MRI. J. Appl. Physiol. 117:1084–1089.
55. Wieling, W., and J. J. Van Lieshout. 1997. Maintenance of postural normotension in humans. Pp. 73–82 in P. A. Low, ed. Clinical autonomic disorders (2 edn). Little Brown and Company, Boston.