Impaired dynamic cerebral autoregulation at rest and during isometric exercise in type 2 diabetes patients

American Journal of Physiology - Heart and Circulatory Physiology

Volumn 308, Issue 7, 2015, Pages 681-687

  Vianna, Lauro C ^a,b   Deo, Shekhar H ^b   Jensen, Areum K ^b   Holwerda, Seth W ^b   Zimmerman, Matthew C ^d   Fadel, Paul J ^b,c  

^a UNIVERSITY OF BRASILIA   (Brazil)

^b University of Missouri   (United States)

^c UNIVERSITY OF MISSOURI   (United States)

^d UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

Author keywords

Cerebral blood flow; Oxidative stress; Reactive oxygen species; Static handgrip

Indexed keywords

GLUCOSE; HEMOGLOBIN A1C; REACTIVE OXYGEN METABOLITE; SUPEROXIDE;

ADULT; ARTERIAL PRESSURE; ARTICLE; AUTOREGULATION; BLOOD FLOW VELOCITY; BLOOD PRESSURE MEASUREMENT; BRAIN BLOOD FLOW; BREATHING MECHANICS; CARBON DIOXIDE TENSION; CARDIOVASCULAR RESPONSE; CEREBRAL AUTOREGULATION; CLINICAL ARTICLE; CONTROLLED STUDY; DIABETIC PATIENT; ELECTROCARDIOGRAM; FEMALE; GLUCOSE BLOOD LEVEL; HAND GRIP; HUMAN; HYPERTENSION; ISOMETRIC EXERCISE; MALE; MEAN ARTERIAL PRESSURE; MIDDLE CEREBRAL ARTERY; MUSCLE ISOMETRIC CONTRACTION; NON INSULIN DEPENDENT DIABETES MELLITUS; OXIDATIVE STRESS; PHOTOELECTRIC PLETHYSMOGRAPHY; PRIORITY JOURNAL; REST; RESTING HEART RATE; BLOOD; BRAIN CIRCULATION; CASE CONTROL STUDY; CEREBROVASCULAR DISORDERS; COMPLICATION; DIABETES MELLITUS, TYPE 2; DIABETIC ANGIOPATHIES; EXERCISE; HAND STRENGTH; HEART RATE; HOMEOSTASIS; METABOLISM; MIDDLE AGED; PATHOPHYSIOLOGY; TIME;

ARTERIAL PRESSURE; BLOOD FLOW VELOCITY; CASE-CONTROL STUDIES; CEREBROVASCULAR CIRCULATION; CEREBROVASCULAR DISORDERS; DIABETES MELLITUS, TYPE 2; DIABETIC ANGIOPATHIES; EXERCISE; FEMALE; HAND STRENGTH; HEART RATE; HOMEOSTASIS; HUMANS; HYPERTENSION; ISOMETRIC CONTRACTION; MALE; MIDDLE AGED; MIDDLE CEREBRAL ARTERY; OXIDATIVE STRESS; SUPEROXIDES; TIME FACTORS;

EID: 84926320348     PISSN: 03636135     EISSN: 15221539     Source Type: Journal    
DOI: 10.1152/ajpheart.00343.2014     Document Type: Article

References (56)

1. Aaslid R, Lindegaard KF, Sorteberg W, Nornes H. Cerebral autoregulation dynamics in humans. Stroke 20: 45-52, 1989.
2. Alessio HM, Hagerman AE, Fulkerson BK, Ambrose J, Rice RE, Wiley RL. Generation of reactive oxygen species after exhaustive aerobic and isometric exercise. Med Sci Sports Exerc 32: 1576-1581, 2000.
3. Bailey DM, Evans KA, McEneny J, Young IS, Hullin DA, James PE, Ogoh S, Ainslie PN, Lucchesi C, Rockenbauer A, Culcasi M, Pietri S. Exercise-induced oxidative-nitrosative stress is associated with impaired dynamic cerebral autoregulation and blood-brain barrier leakage. Exp Physiol 96: 1196-1207, 2011.
4. Beckman JS, Koppenol WH. Nitric oxide, superoxide, and peroxynitrite: the good, the bad, ugly. Am J Physiol Cell Physiol 271: C1424-C1437, 1996.
5. Bor-Seng-Shu E, Kita WS, Figueiredo EG, Paiva WS, Fonoff ET, Teixeira MJ, Panerai RB. Cerebral hemodynamics: concepts of clinical importance. Arq Neuropsiquiatr 70: 352-356, 2012.
6. Brown CM, Marthol H, Zikeli U, Ziegler D, Hilz MJ. A simple deep breathing test reveals altered cerebral autoregulation in type 2 diabetic patients. Diabetologia 51: 756-761, 2008.
7. Credeur DP, Holwerda SW, Boyle LJ, Vianna LC, Jensen AK, Fadel PJ. Effect of aging on carotid baroreflex control of blood pressure and leg vascular conductance in women. Am J Physiol Heart Circ Physiol 306: H1417-H1425, 2014.
8. Deo SH, Fisher JP, Vianna LC, Kim A, Chockalingam A, Zimmerman MC, Zucker IH, Fadel PJ. Statin therapy lowers muscle sympathetic nerve activity and oxidative stress in patients with heart failure. Am J Physiol Heart Circ Physiol 303: H377-H385, 2012.
9. Erdos B, Snipes JA, Miller AW, Busija DW. Cerebrovascular dysfunction in Zucker obese rats is mediated by oxidative stress and protein kinase C. Diabetes 53: 1352-1359, 2004.
10. Fadel PJ, Wang Z, Tuncel M, Watanabe H, Abbas A, Arbique D, Vongpatanasin W, Haley RW, Victor RG, Thomas GD. Reflex sympathetic activation during static exercise is severely impaired in patients with myophosphorylase deficiency. J Physiol 548: 983-993, 2003.
11. Fisher JP, Ogoh S, Young CN, Raven PB, Fadel PJ. Regulation of middle cerebral artery blood velocity during dynamic exercise in humans: influence of aging. J Appl Physiol (1985) 105: 266-273, 2008.
12. Guo ZN, Liu J, Xing Y, Yan S, Lv C, Jin H, Yang Y. Dynamic cerebral autoregulation is heterogeneous in different subtypes of acute ischemic stroke. PLoS One 9: e93213, 2014.
13. Harms MP, Wesseling KH, Pott F, Jenstrup M, Van Goudoever J, Secher NH, Van Lieshout JJ. Continuous stroke volume monitoring by modelling flow from non-invasive measurement of arterial pressure in humans under orthostatic stress. Clin Sci (Lond) 97: 291-301, 1999.
14. Hogikyan RV, Galecki AT, Halter JB, Supiano MA. Heightened norepinephrine-mediated vasoconstriction in type 2 diabetes. Metabolism 48: 1536-1541, 1999.
15. Huggett RJ, Scott EM, Gilbey SG, Stoker JB, Mackintosh AF, Mary DA. Impact of type 2 diabetes mellitus on sympathetic neural mechanisms in hypertension. Circulation 108: 3097-3101, 2003.
16. Huq R, Philbey CE, Mistri AK, Panerai RB, Robinson TG. Dynamic cerebral autoregulation assessed by respiratory manoeuvres in non-insulintreated Type 2 diabetes mellitus. Diabet Med 29: 609-613, 2012.
17. Immink RV, van Montfrans GA, Stam J, Karemaker JM, Diamant M, van Lieshout JJ. Dynamic cerebral autoregulation in acute lacunar and middle cerebral artery territory ischemic stroke. Stroke 36: 2595-2600, 2005.
18. Irani K. Oxidant signaling in vascular cell growth, death, and survival: a review of the roles of reactive oxygen species in smooth muscle and endothelial cell mitogenic and apoptotic signaling. Circ Res 87: 179-183, 2000.
19. Johnson PC, Brendel K, Meezan E. Thickened cerebral cortical capillary basement membranes in diabetics. Arch Pathol Lab Med 106: 214-217, 1982.
20. Jordan J, Shannon JR, Black BK, Paranjape SY, Barwise J, Robertson D. Raised cerebrovascular resistance in idiopathic orthostatic intolerance: evidence for sympathetic vasoconstriction. Hypertension 32: 699-704, 1998.
21. Jordan JD, Powers WJ. Cerebral autoregulation and acute ischemic stroke. Am J Hypertens 25: 946-950, 2012.
22. Joyner WL, Mayhan WG, Johnson RL, Phares CK. Microvascular alterations develop in Syrian hamsters after the induction of diabetes mellitus by streptozotocin. Diabetes 30: 93-100, 1981.
23. Kim YS, Immink RV, Stok WJ, Karemaker JM, Secher NH, van Lieshout JJ. Dynamic cerebral autoregulatory capacity is affected early in Type 2 diabetes. Clin Sci (Lond) 115: 255-262, 2008.
24. Kim YS, Secher NH, van Lieshout JJ. Resistance exercise and control of cerebral blood flow in type 2 diabetes. Diabetologia 51: 1755-1756, 2008.
25. Kingwell BA, Formosa M, Muhlmann M, Bradley SJ, McConell GK. Type 2 diabetic individuals have impaired leg blood flow responses to exercise: role of endothelium-dependent vasodilation. Diabetes Care 26: 899-904, 2003.
26. Kissela BM, Khoury J, Kleindorfer D, Woo D, Schneider A, Alwell K, Miller R, Ewing I, Moomaw CJ, Szaflarski JP, Gebel J, Shukla R, Broderick JP. Epidemiology of ischemic stroke in patients with diabetes: the greater Cincinnati/Northern Kentucky Stroke Study. Diabetes Care 28: 355-359, 2005.
27. Long AN, Dagogo-Jack S. Comorbidities of diabetes and hypertension: mechanisms and approach to target organ protection. J Clin Hypertens (Greenwich) 13: 244-251, 2011.
28. MacDougall JD, Tuxen D, Sale DG, Moroz JR, Sutton JR. Arterial blood pressure response to heavy resistance exercise. J Appl Physiol (1985) 58: 785-790, 1985.
29. Mark AL, Victor RG, Nerhed C, Wallin BG. Microneurographic studies of the mechanisms of sympathetic nerve responses to static exercise in humans. Circ Res 57: 461-469, 1985.
30. Marthol H, Zikeli U, Brown CM, Tutaj M, Hilz MJ. Cardiovascular and cerebrovascular responses to lower body negative pressure in type 2 diabetic patients. J Neurol Sci 252: 99-105, 2007.
31. Marwick TH, Hordern MD, Miller T, Chyun DA, Bertoni AG, Blumenthal RS, Philippides G, Rocchini A. Exercise training for type 2 diabetes mellitus: impact on cardiovascular risk: a scientific statement from the American Heart Association. Circulation 119: 3244-3262, 2009.
32. Mikus CR, Fairfax ST, Libla JL, Boyle LJ, Vianna LC, Oberlin DJ, Uptergrove GM, Deo SH, Kim A, Kanaley JA, Fadel PJ, Thyfault JP. Seven days of aerobic exercise training improves conduit artery blood flow following glucose ingestion in patients with type 2 diabetes. J Appl Physiol (1985) 111: 657-664, 2011.
33. Nazir FS, Alem M, Small M, Connell JM, Lees KR, Walters MR, Cleland SJ. Blunted response to systemic nitric oxide synthase inhibition in the cerebral circulation of patients with Type 2 diabetes. Diabet Med 23: 398-402, 2006.
34. Ogoh S, Brothers RM, Eubank WL, Raven PB. Autonomic neural control of the cerebral vasculature: acute hypotension. Stroke 39: 1979-1987, 2008.
35. Ogoh S, Dalsgaard MK, Yoshiga CC, Dawson EA, Keller DM, Raven PB, Secher NH. Dynamic cerebral autoregulation during exhaustive exercise in humans. Am J Physiol Heart Circ Physiol 288: H1461-H1467, 2005.
36. Ogoh S, Fisher JP, Young CN, Raven PB, Fadel PJ. Transfer function characteristics of the neural and peripheral arterial baroreflex arcs at rest and during postexercise muscle ischemia in humans. Am J Physiol Heart Circ Physiol 296: H1416-H1424, 2009.
37. Ogoh S, Sato K, Akimoto T, Oue A, Hirasawa A, Sadamoto T. Dynamic cerebral autoregulation during and after handgrip exercise in humans. J Appl Physiol (1985) 108: 1701-1705, 2010.
38. Pena Silva RA, Chu Y, Miller JD, Mitchell IJ, Penninger JM, Faraci FM, Heistad DD. Impact of ACE2 deficiency and oxidative stress on cerebrovascular function with aging. Stroke 43: 3358-3363, 2012.
39. Reinhard M, Roth M, Guschlbauer B, Harloff A, Timmer J, Czosnyka M, Hetzel A. Dynamic cerebral autoregulation in acute ischemic stroke assessed from spontaneous blood pressure fluctuations. Stroke 36: 1684-1689, 2005.
40. Reinhard M, Wihler C, Roth M, Harloff A, Niesen WD, Timmer J, Weiller C, Hetzel A. Cerebral autoregulation dynamics in acute ischemic stroke after rtPA thrombolysis. Cerebrovasc Dis 26: 147-155, 2008.
41. Sanya EO, Brown CM, Dutsch M, Zikeli U, Neundorfer B, Hilz MJ. Impaired cardiovagal and vasomotor responses to baroreceptor stimulation in type II diabetes mellitus. Eur J Clin Invest 33: 582-588, 2003.
42. Secher NH, Seifert T, Van Lieshout JJ. Cerebral blood flow and metabolism during exercise: implications for fatigue. J Appl Physiol (1985) 104: 306-314, 2008.
43. Shi X, Gallagher KM, SASM, Bryant KH, Raven PB. Diminished forearm vasomotor response to central hypervolemic loading in aerobically fit individuals. Med Sci Sports Exerc 28: 1388-1395, 1996.
44. Sowers JR, Epstein M. Diabetes mellitus and associated hypertension, vascular disease, and nephropathy. An update. Hypertension 26: 869-879, 1995.
45. Thaning P, Bune LT, Hellsten Y, Pilegaard H, Saltin B, Rosenmeier JB. Attenuated purinergic receptor function in patients with type 2 diabetes. Diabetes 59: 182-189, 2010.
46. Thaning P, Bune LT, Zaar M, Saltin B, Rosenmeier JB. Functional sympatholysis during exercise in patients with type 2 diabetes with intact response to acetylcholine. Diabetes Care 34: 1186-1191, 2011.
47. Tiecks FP, Lam AM, Aaslid R, Newell DW. Comparison of static and dynamic cerebral autoregulation measurements. Stroke 26: 1014-1019, 1995.
48. Tobias DK, Pan A, Jackson CL, O’Reilly EJ, Ding EL, Willett WC, Manson JE, Hu FB. Body-mass index and mortality among adults with incident type 2 diabetes. N Engl J Med 370: 233-244, 2014.
49. Tzeng YC, Ainslie PN. Blood pressure regulation IX: cerebral autoregulation under blood pressure challenges. Eur J Appl Physiol 114: 545-559, 2014.
50. Tzeng YC, Willie CK, Atkinson G, Lucas SJ, Wong A, Ainslie PN. Cerebrovascular regulation during transient hypotension and hypertension in humans. Hypertension 56: 268-273, 2010.
51. Vianna LC, Araujo CG, Fisher JP. Influence of central command and muscle afferent activation on anterior cerebral artery blood velocity responses to calf exercise in humans. J Appl Physiol (1985) 107: 1113-1120, 2009.
52. Vianna LC, Hart EC, Fairfax ST, Charkoudian N, Joyner MJ, Fadel PJ. Influence of age and sex on the pressor response following a spontaneous burst of muscle sympathetic nerve activity. Am J Physiol Heart Circ Physiol 302: H2419-H2427, 2012.
53. Vianna LC, Sales AR, da Nobrega AC. Cerebrovascular responses to cold pressor test during static exercise in humans. Clin Physiol Funct Imaging 32: 59-64, 2012.
54. Victor RG, Seals DR, Mark AL. Differential control of heart rate and sympathetic nerve activity during dynamic exercise. Insight from intraneural recordings in humans. J Clin Invest 79: 508-516, 1987.
55. Zhang R, Zuckerman JH, Iwasaki K, Wilson TE, Crandall CG, Levine BD. Autonomic neural control of dynamic cerebral autoregulation in humans. Circulation 106: 1814-1820, 2002.
56. Zhao W, Katzmarzyk PT, Horswell R, Wang Y, Johnson J, Hu G. Sex differences in the risk of stroke and HbA among diabetic patients. Diabetologia 57: 918-926, 2014.