Train the vessel, gain the brain: Physical activity and vessel function and the impact on stroke prevention and outcome in cerebrovascular disease

Cerebrovascular Diseases

Volumn 35, Issue 4, 2013, Pages 303-312

  Schmidt, Wolf ^a   Endres, Matthias ^a   Dimeo, Fernando ^a   Jungehulsing, Gerhard J ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Angiogenesis; Arteriogenesis; Cerebral blood flow; Neovascularization; Neurogenesis; Physical activity

Indexed keywords

NITRIC OXIDE;

ANGIOGENESIS; AUTOREGULATION; BIOAVAILABILITY; BLOOD VESSEL FUNCTION; BRAIN BLOOD FLOW; CD34 SELECTION; CEREBROVASCULAR ACCIDENT; CEREBROVASCULAR DISEASE; COGNITION; COLLATERAL CIRCULATION; ENDOTHELIAL PROGENITOR CELL; EXERCISE INTENSITY; HUMAN; OUTCOME ASSESSMENT; PHYSICAL ACTIVITY; PRIMARY PREVENTION; PRIORITY JOURNAL; REVIEW; SHEAR STRESS;

EID: 84876092549     PISSN: 10159770     EISSN: 14219786     Source Type: Journal    
DOI: 10.1159/000347061     Document Type: Review

References (118)

1. Physical activity and cardiovascular health. NIH Consensus Development Panel on Physical Activity and Cardiovascular Health. JAMA 1996; 276: 241-246.
2. Bluher M, Zimmer P: Metabolic and cardiovascular effects of physical activity, exercise and fitness in patients with type 2. diabetes (in German). Dtsch Med Wochenschr 2010; 135: 930-934.
3. Walther C, Gielen S, Hambrecht R: The effect of exercise training on endothelial function in cardiovascular disease in humans. Exerc Sport Sci Rev 2004; 32: 129-134.
4. Maiorana A, et al: Exercise and the nitric oxide vasodilator system. Sports Med 2003; 33: 1013-1035.
5. Hambrecht R, et al: Regular physical activity improves endothelial function in patients with coronary artery disease by increasing phosphorylation of endothelial nitric oxide synthase. Circulation 2003; 107: 3152-3158.
6. Hambrecht R, et al: Regular physical exercise corrects endothelial dysfunction and improves exercise capacity in patients with chronic heart failure. Circulation 1998; 98: 2709-2715.
7. Endres M, et al: Mechanisms of stroke protection by physical activity. Ann Neurol 2003; 54: 582-590.
8. Rolland Y, van Kan GA, Vellas B: Healthy brain aging: role of exercise and physical activity. Clin Geriatr Med 2010; 26: 75-87.
9. Leung FP, et al: Exercise, vascular wall and cardiovascular diseases: an update. Part 1. Sports Med 2008; 38: 1009-1024.
10. Reinhard, M, et al: Dynamic cerebral autoregulation and collateral flow patterns in patients with severe carotid stenosis or occlusion. Ultrasound Med Biol 2003; 29: 1105-1113.
11. Lassen NA: Cerebral blood flow and oxygen consumption in man. Physiol Rev 1959; 39: 183-238.
12. Ozgur HT, et al: Correlation of cerebrovascular reserve as measured by acetazolamidechallenged SPECT with angiographic flow patterns and intra-or extracranial arterial stenosis. AJNR Am J Neuroradiol 2001; 22: 928-936.
13. Vernieri F, et al: Effect of collateral blood flow and cerebral vasomotor reactivity on the outcome of carotid artery occlusion. Stroke 2001; 32: 1552-1558.
14. Widder B, Kleiser B, Krapf H: Course of cerebrovascular reactivity in patients with carotid artery occlusions. Stroke 1994; 25: 1963-1967.
15. Markus H, Cullinane M: Severely impaired cerebrovascular reactivity predicts stroke and TIA risk in patients with carotid artery stenosis and occlusion. Brain 2001; 124: 457-467.
16. Liebeskind DS: Collateral circulation. Stroke 2003; 34: 2279-2284.
17. Lindegaard KF, et al: Assessment of intracranial hemodynamics in carotid artery disease by transcranial Doppler ultrasound. J Neurosurg 1985; 63: 890-898.
18. Bisschops RH, et al: Collateral flow and ischemic brain lesions in patients with unilateral carotid artery occlusion. Neurology 2003; 60: 1435-1441.
19. Hendrikse J, Eikelboom BC, van der Grond J: Magnetic resonance angiography of collateral compensation in asymptomatic and symptomatic internal carotid artery stenosis. J Vasc Surg 2002; 36: 799-805.
20. Arras M, et al: Monocyte activation in angiogenesis and collateral growth in the rabbit hindlimb. J Clin Invest 1998; 101: 40-50.
21. Schaper W, De Brabander M, Lewi P: DNA synthesis and mitoses in coronary collateral vessels of the dog. Circ Res 1971; 28: 671-679.
22. Busch HJ, et al: Arteriogenesis in hypoperfused rat brain. J Cereb Blood Flow Metab 2003; 23: 621-628.
23. Buschmann IR, et al: Therapeutic induction of arteriogenesis in hypoperfused rat brain via granulocyte-macrophage colony-stimulating factor. Circulation 2003; 108: 610-615.
24. Hoefer IE, et al: Time course of arteriogenesis following femoral artery occlusion in the rabbit. Cardiovasc Res 2001; 49: 609-617.
25. Grines CL, et al: Angiogenic Gene Therapy (AGENT) Trial in patients with stable angina pectoris. Circulation 2002; 105: 1291-1297.
26. Simons M, et al: Pharmacological treatment of coronary artery disease with recombinant fibroblast growth factor-2: double-blind, randomized, controlled clinical trial. Circulation 2002; 105: 788-793.
27. Henry TD, et al: The VIVA Trial: vascular endothelial growth factor in ischemia for vascular angiogenesis. Circulation 2003; 107: 1359-1365.
28. Rajagopalan S, et al: Regional angiogenesis with vascular endothelial growth factor in peripheral arterial disease: a phase II randomized, double-blind, controlled study of adenoviral delivery of vascular endothelial growth factor 121 in patients with disabling intermittent claudication. Circulation 2003; 108: 1933-1938.
29. Seiler C, et al: Promotion of collateral growth by granulocyte-macrophage colony-stimulating factor in patients with coronary artery disease: a randomized, double-blind, placebocontrolled study. Circulation 2001; 104: 2012-2017.
30. van Royen N, et al: START Trial: a pilot study on stimulation of arteriogenesis using subcutaneous application of granulocyte-macrophage colony-stimulating factor as a new treatment for peripheral vascular disease. Circulation 2005; 112: 1040-1046.
31. Zbinden S, et al: Safety and efficacy of subcutaneous-only granulocyte-macrophage colony-stimulating factor for collateral growth promotion in patients with coronary artery disease. J Am Coll Cardiol 2005; 46: 1636-1642.
32. Schabitz WR, et al: AXIS: a trial of intravenous granulocyte colony-stimulating factor in acute ischemic stroke. Stroke 2010; 41: 2545-2551.
33. Schierling W, et al: Increased intravascular flow rate triggers cerebral arteriogenesis. J Cereb Blood Flow Metab 2009; 29: 726-737.
34. Heil M, Schaper W: Influence of mechanical, cellular, and molecular factors on collateral artery growth (arteriogenesis). Circ Res 2004; 95: 449-458.
35. Schaper W: Collateral circulation: past and present. Basic Res Cardiol 2009; 104: 5-21.
36. Risau W: Mechanisms of angiogenesis. Nature 1997; 386: 671-674.
37. Gertz K, et al: Physical activity improves longterm stroke outcome via endothelial nitric oxide synthase-dependent augmentation of neovascularization and cerebral blood flow. Circ Res 2006; 99: 1132-1140.
38. Li Calzi S, et al: EPCs and pathological angiogenesis: when good cells go bad. Microvasc Res 2010; 79: 207-216.
39. Shantsila E, Watson T, Lip GY: Endothelial progenitor cells in cardiovascular disorders. J Am Coll Cardiol 2007; 49: 741-752.
40. Hristov M, Weber C: Endothelial progenitor cells: characterization, pathophysiology, and possible clinical relevance. J Cell Mol Med 2004; 8: 498-508.
41. Peichev M, et al: Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors. Blood 2000; 95: 952-958.
42. Rafii S, Lyden D: Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med 2003; 9: 702-712.
43. Werner N, et al: Endothelial progenitor cells correlate with endothelial function in patients with coronary artery disease. Basic Res Cardiol 2007; 102: 565-571.
44. Hill JM, et al: Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med 2003; 348: 593-600.
45. Werner N, et al: Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med 2005; 353: 999-1007.
46. Yoshihara T, et al: Increase in circulating CD34-positive cells in patients with angiographic evidence of moyamoya-like vessels. J Cereb Blood Flow Metab 2008; 28: 1086-1089.
47. Adams V, et al: Increase of circulating endothelial progenitor cells in patients with coronary artery disease after exercise-induced ischemia. Arterioscler Thromb Vasc Biol 2004; 24: 684-690.
48. Rehman J, et al: Exercise acutely increases circulating endothelial progenitor cells and mono cyte/macrophage-derived angiogenic cells. J Am Coll Cardiol 2004; 43: 2314-2318.
49. Laufs U, et al: Physical training increases endothelial progenitor cells, inhibits neointima formation, and enhances angiogenesis. Circulation 2004; 109: 220-226.
50. Sandri M, et al: Effects of exercise and ischemia on mobilization and functional activation of blood-derived progenitor cells in patients with ischemic syndromes: results of 3. randomized studies. Circulation 2005; 111: 3391-3399.
51. Palmer TD, Willhoite AR, Gage FH: Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 2000; 425: 479-494.
52. Segura I, et al: The neurovascular link in health and disease: an update. Trends Mol Med 2009; 15: 439-451.
53. Carmeliet P, Jain RK: Molecular mechanisms and clinical applications of angiogenesis. Nature 2011; 473: 298-307.
54. Leventhal C, et al: Endothelial trophic support of neuronal production and recruitment from the adult mammalian subependyma. Mol Cell Neurosci 1999; 13: 450-464.
55. Quinones-Hinojosa A, et al: Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J Comp Neurol 2006; 494: 415-434.
56. Wiltrout C, et al: Repairing brain after stroke: a review on post-ischemic neurogenesis. Neurochem Int 2007; 50: 1028-1041.
57. Garcia-Verdugo JM, et al: Architecture and cell types of the adult subventricular zone: in search of the stem cells. J Neurobiol 1998; 36: 234-248.
58. Ohab JJ, et al: A neurovascular niche for neurogenesis after stroke. J Neurosci 2006; 26: 13007-13016.
59. Teng H, et al: Coupling of angiogenesis and neurogenesis in cultured endothelial cells and neural progenitor cells after stroke. J Cereb Blood Flow Metab 2008; 28: 764-771.
60. Pereira AC, et al: An in vivo correlate of exercise-induced neurogenesis in the adult dentate gyrus. Proc Natl Acad Sci USA 2007; 104: 5638-5643.
61. Van der Borght K, et al: Physical exercise leads to rapid adaptations in hippocampal vasculature: temporal dynamics and relationship to cell proliferation and neurogenesis. Hippocampus 2009; 19: 928-936.
62. van Praag H, Kempermann G, Gage FH: Running increases cell proliferation and neurogenesis in the adult mouse dentate gyrus. Nat Neurosci 1999; 2: 266-270.
63. van Praag H, et al: Exercise enhances learning and hippocampal neurogenesis in aged mice. J Neurosci 2005; 25: 8680-8685.
64. Seevinck PR, Deddens LH, Dijkhuizen RM: Magnetic resonance imaging of brain angiogenesis after stroke. Angiogenesis 2010; 13: 101-111.
65. Aronen HJ, et al: High microvascular blood volume is associated with high glucose uptake and tumor angiogenesis in human gliomas. Clin Cancer Res 2000; 6: 2189-2200.
66. Goldman SA, Chen Z: Perivascular instruction of cell genesis and fate in the adult brain. Nat Neurosci 2011; 14: 1382-1389.
67. Ding YH, et al: Exercise preconditioning ameliorates inflammatory injury in ischemic rats during reperfusion. Acta Neuropathol 2005; 109: 237-246.
68. Yang YR, Wang RY, Wang PS: Early and late treadmill training after focal brain ischemia in rats. Neurosci Lett 2003; 339: 91-94.
69. Ding Y, et al: Exercise pre-conditioning reduces brain damage in ischemic rats that may be associated with regional angiogenesis and cellular overexpression of neurotrophin. Neuroscience 2004; 124: 583-591.
70. Deplanque D, et al: Prior TIA, lipid-lowering drug use, and physical activity decrease ischemic stroke severity. Neurology 2006; 67: 1403-1410.
71. Stroud N, et al: Prestroke physical activity and early functional status after stroke. J Neurol Neurosurg Psychiatry 2009; 80: 1019-1022.
72. Krarup LH, et al: Prestroke physical activity is associated with severity and long-term outcome from first-ever stroke. Neurology 2008; 71: 1313-1318.
73. Lautenschlager NT, Cox K, Kurz AF: Physical activity and mild cognitive impairment and Alzheimer's disease. Curr Neurol Neurosci Rep 2010; 10: 352-358.
74. Ries ML, et al: Magnetic resonance imaging characterization of brain structure and function in mild cognitive impairment: a review. J Am Geriatr Soc 2008; 56: 920-934.
75. Hoth KF, et al: Endothelial function and white matter hyperintensities in older adults with cardiovascular disease. Stroke 2007; 38: 308-312.
76. Iadecola C, Gorelick PB: Converging pathogenic mechanisms in vascular and neurodegenerative dementia. Stroke 2003; 34: 335-337.
77. Aarsland D, et al: Is physical activity a potential preventive factor for vascular dementia? A systematic review. Aging Ment Health 2010; 14: 386-395.
78. Hamer M, Chida Y: Physical activity and risk of neurodegenerative disease: a systematic review of prospective evidence. Psychol Med 2009; 39: 3-11.
79. Angevaren M, et al: Physical activity and enhanced fitness to improve cognitive function in older people without known cognitive impairment. Cochrane Database Syst Rev 2008:CD005381.
80. Vaynman S, Gomez-Pinilla F: Revenge of the 'sit': how lifestyle impacts neuronal and cognitive health through molecular systems that interface energy metabolism with neuronal plasticity. J Neurosci Res 2006; 84: 699-715.
81. Colcombe SJ, et al: Aerobic fitness reduces brain tissue loss in aging humans. J Gerontol A Biol Sci Med Sci 2003; 58: 176-180.
82. Kleim JA, Cooper NR, VandenBerg PM: Exercise induces angiogenesis but does not alter movement representations within rat motor cortex. Brain Res 2002; 934: 1-6.
83. McMorris T, et al: A test of the catecholamines hypothesis for an acute exercise-cognition interaction. Pharmacol Biochem Behav 2008; 89: 106-115.
84. Kubesch S, et al: Aerobic endurance exercise improves executive functions in depressed patients. J Clin Psychiatry 2003; 64: 1005-1012.
85. Hillman CH, Snook EM, Jerome GJ: Acute cardiovascular exercise and executive control fun ction. Int J Psychophysiol 2003; 48: 307-314.
86. Kamijo K, et al: The interactive effect of exercise intensity and task difficulty on human cognitive processing. Int J Psychophysiol 2007; 65: 114-121.
87. Ploughman M, et al: Endurance exercise regimens induce differential effects on brainderived neurotrophic factor, synapsin-I and insulin-like growth factor I after focal ischemia. Neuroscience 2005; 136: 991-1001.
88. Ma Q: Beneficial effects of moderate voluntary physical exercise and its biological mechanisms on brain health. Neurosci Bull 2008; 24: 265-270
89. Flöel A, et al: Physical activity and memory functions: are neurotrophins and cerebral gray matter volume the missing link? Neuroimage 2756-2756. 2010 49
90. Ruscheweyh R, et al: Physical activity and memory functions: an interventional study. Neurobiol Aging 2011; 32: 1304-1319.
91. Brosse AL, et al: Exercise and the treatment of clinical depression in adults: recent findings and future directions. Sports Med 2002; 32: 741-760
92. Stewart KJ, et al. Are fitness, activity, and fatness associated with health-related quality of life and mood in older persons? J Cardiopulm Rehabil 2003 23 115-115.
93. Stoquart-ElSankari S, et al: Aging effects on cerebral blood and cerebrospinal fluid flows. J Cereb Blood Flow Metab 2007; 27: 1563-1572.
94. Beason-Held LL, et al: Longitudinal changes in cerebral blood flow in the older hypertensive brain. Stroke 2007; 38: 1766-1773.
95. Ainslie PN, et al: Elevation in cerebral blood flow velocity with aerobic fitness throughout healthy human ageing. J Physiol 2008; 586: 4005-4010.
96. van Beek AH, et al: Cerebral autoregulation: an overview of current concepts and methodology with special focus on the elderly. J Cereb Blood Flow Metab 2008; 28: 1071-1085.
97. Abbott RD, et al: Physical activity in older middle-aged men and reduced risk of stroke: the Honolulu Heart Program. Am J Epidemiol 1994; 139: 881-893.
98. Haheim LL, et al: Risk factors of stroke incidence and mortality. A 12-year follow-up of the Oslo Study. Stroke 1993; 24: 1484-1489.
99. Hu FB, et al: Physical activity and risk of stroke in women. JAMA 2000; 283: 2961-2967.
100. Sattelmair JR, et al: Physical activity and risk of stroke in women. Stroke 2010; 41: 1243-1250.
101. Gillum RF, Mussolino ME, Ingram DD: Physical activity and stroke incidence in women and men: the NHANES I Epidemiologic Follow-up Study. Am J Epidemiol 1996; 143: 860-869.
102. Sacco RL, et al: Leisure-time physical activity and ischemic stroke risk: the Northern Manhattan Stroke Study. Stroke 1998; 29: 380-387.
103. Ellekjar H, et al: Physical activity and stroke mortality in women: ten-year follow-up of the Nord-Trondelag Health Survey 1984-1986. Stroke 2000; 31: 14-18.
104. Hu G, et al: Leisure time, occupational, and commuting physical activity and the risk of stroke. Stroke 2005; 36: 1994-1999.
105. Evenson KR, et al: Physical activity and ischemic stroke risk: the Atherosclerosis Risk in Communities Study. Stroke 1999; 30: 1333-1339.
106. Lee I-M, Paffenbarger RS Jr: Physical activity and stroke incidence: the Harvard Alumni Health Study. Stroke 1998; 29: 2049-2054.
107. Lee IM, et al: Exercise and risk of stroke in male physicians. Stroke 1999; 30: 1-6.
108. Lee CD, Folsom AR, Blair SN: Physical activity and stroke risk: a meta-analysis. Stroke 2003; 34: 2475-2481.
109. Wendel-Vos G, et al: Physical activity and stroke. A meta-analysis of observational data. Int J Epidemiol 2004; 33: 787-798.
110. Lee IM, et al: Exercise and risk of stroke in male physicians. Stroke 1999; 30: 1-6.
111. Wannamethee G, Shaper AG: Physical activity and stroke in British middle-aged men. BMJ 1992; 304: 597-601.
112. Aizer A, et al: Relation of vigorous exercise to risk of atrial fibrillation. Am J Cardiol 2009; 103: 1572-1577.
113. Mozaffarian D, et al: Physical activity and incidence of atrial fibrillation in older adults: the Cardiovascular Health Study. Circulation 2008; 118: 800-807.
114. Willey JZ, et al: Physical activity and risk of ischemic stroke in the Northern Manhattan Study. Neurology 2009; 73: 1774-1779.
115. Grau AJ, et al: Association between recent sports activity, sports activity in young adulthood, and stroke. Stroke 2009; 40: 426-431.
116. Saunders DH, et al: Physical fitness training for stroke patients. Cochrane Database Syst Rev 2009:CD003316.
117. Cheng E, et al: Comparison of secondary prevention care after myocardial infarction and stroke. Cerebrovasc Dis 2006; 21: 235-241.
118. Cornelissen VA, Fagard RH: Effect of resistance training on resting blood pressure: a meta-analysis of randomized controlled trials. J Hypertens 2005; 23: 251-259.