Further understanding of cerebral autoregulation at the bedside: Possible implications for future therapy

Expert Review of Neurotherapeutics

Volumn 15, Issue 2, 2014, Pages 169-185

  Donnelly, Joseph ^a   Aries, Marcel J ^a,b   Czosnyka, Marek ^a,c  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY MEDICAL CENTER GRONINGEN   (Netherlands)

^c WARSAW UNIVERSITY OF TECHNOLOGY   (Poland)

Author keywords

Cerebral autoregulation; Cerebral blood flow; Cerebral perfusion pressure; Critical care medicine; Intracranial pressure; Near infrared spectroscopy; Stroke; Subarachnoid hemorrhage; Traumatic brain injury; Ultrasound

Indexed keywords

ASSISTED VENTILATION; AUTOREGULATION; BRAIN BLOOD FLOW; BRAIN ISCHEMIA; BRAIN PERFUSION; CARDIOPULMONARY BYPASS; CAROTID ARTERY OBSTRUCTION; HUMAN; HYDROCEPHALUS; NEUROPROTECTION; PATIENT POSITIONING; PERFUSION PRESSURE; PHYSIOLOGICAL PROCESS; PREMATURITY; REVIEW; SUBARACHNOID HEMORRHAGE; TRAUMATIC BRAIN INJURY; ANIMAL; BLOOD PRESSURE; BRAIN; BRAIN CIRCULATION; BRAIN INJURIES; HOMEOSTASIS; INTRACRANIAL PRESSURE; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANIMALS; BLOOD PRESSURE; BRAIN; BRAIN INJURIES; CEREBROVASCULAR CIRCULATION; HOMEOSTASIS; HUMANS; INTRACRANIAL PRESSURE;

EID: 84921720299     PISSN: 14737175     EISSN: 17448360     Source Type: Journal    
DOI: 10.1586/14737175.2015.996552     Document Type: Review

References (112)

1. Willie CK, Colino FL, Bailey DM, et al. Utility of transcranial Doppler ultrasound for the integrative assessment of cerebrovascular function. J Neurosci Methods 2011;196(2):221-37
2. Czosnyka M, Brady K, Reinhard M, et al. Monitoring of cerebrovascular autoregulation: facts, myths, and missing links. Neurocrit Care 2009;10(3):373-86
3. Aries MJH, Elting JW, De Keyser J, et al. Cerebral autoregulation in stroke a review of transcranial Doppler studies. Stroke 2010;41:2697-704
4. Peterson ECE, Wang Z, Britz G. Regulation of cerebral blood flow. Int J Vasc Med 2011;2011
5. Palomares SM, Cipolla MJ. Myogenic tone as a therapeutic target for ischemic stroke. Curr Vasc Pharmacol 2013. [Epub ahead of print]
6. Ter Laan M, van Dijk JMC, Elting JW, et al. Sympathetic regulation of cerebral blood flow in humans: a review. Br J Anaesth 2013;111(3):361-7
7. Tzeng Y-C, Ainslie PN. Blood pressure regulation IX: cerebral autoregulation under blood pressure challenges. Eur J Appl Physiol 2014;114(3):545-59
8. Jackman K, Iadecola C. Neurovascular regulation in the ischemic brain. Antioxid Redox Signal 2014;00:1-12
9. Willie CK, Tzeng Y-C, Fisher JA, Ainslie PN. Integrative regulation of human brain blood flow. J Physiol 2014;592:841-59
10. Numan T, Bain A, Hoiland R. Static autoregulation in humans: a review and reanalysis. Med Eng Phys 2014;36(11):1487-95
11. Bayliss WM, Hill L, Gulland GL. On Intra-Cranial Pressure and the Cerebral Circulation: part I. Physiological; Part II. Histological J Physiol 1895;18(4):334-62
12. Fog M. The relationship between the blood pressure and the tonic regulation of the pial arteries. J Neurol Psychiatry 1938;1(3):187-97.
13. Harper AM. Autoregulation of cerebral blood flow: influence of the arterial blood pressure on the blood flow through the cerebral cortex. J Neurol Neurosurg Psychiatry 1966;29(5):398-403
14. Lassen N. Cerebral blood flow and oxygen consumption in man. Physiol Rev 1959;39:183-238.
15. Ekström-Jodal B, Häggendal E, Linder L, Nilsson N. Cerebral blood flow autoregulation at high arterial pressures and different levels of carbon dioxide tension in dogs. Eur Neurol 1971;6(1):6-10
16. Kontos HA, Wei EP, Navari RM, et al. Responses of cerebral arteries and arterioles to acute hypotension and hypertension. Am J Physiol 1978;234(4):H371-83.
17. Willie C, Macleod D, Shaw A, et al. Regional brain blood flow in man during acute changes in arterial blood gases. J Physiol 2012;590(Pt 14):3261-75
18. Le Roux P. Physiological monitoring of the severe traumatic brain injury patient in the intensive care unit. Curr Neurol Neurosci Rep 2013;13(3):331
19. Le Roux P, Menon DK, Citerio G, et al. Consensus summary statement of the International Multidisciplinary Consensus Conference on Multimodality Monitoring in Neurocritical Care: A statement for healthcare professionals from the Neurocritical Care Society and the European Society of Intensive. Intensive Care Med 2014;1189-209.
20. Rosner MJ, Rosner SD, Johnson a H. Cerebral perfusion pressure: management protocol and clinical results. J Neurosurg 1995;83(6):949-62
21. Steiner LA, Andrews PJD. Monitoring the injured brain: ICP and CBF. Br J Anaesth 2006;97(1):26-38
22. Aaslid R, Lindegaard KF, Sorteberg W, Nornes H. Cerebral autoregulation dynamics in humans. Stroke 1989;20(1):45-52.
23. Birch AA, Dirnhuber MJ, Hartley-Davies R, et al. Assessment of autoregulation by means of periodic changes in blood pressure. Stroke 1995;26:834-7
24. Diehl RR, Linden D, Lücke D, Berlit P. Phase relationship between cerebral blood flow velocity and blood pressure. A clinical test of autoregulation. Stroke 1995;26:1801-4
25. Zhang R, Zuckerman JH, Giller CA, et al. Transfer function analysis of dynamic cerebral autoregulation in humans. Am J Physiol 1998;274:H233-41
26. Tiecks FP, Lam AM, Aaslid R, Newell DW. Comparison of static and dynamic cerebral autoregulation measurements. Stroke 1995;26(6):1014-19
27. Smirl JD, Lucas SJE, Lewis NCS, et al. Cerebral pressure-flow relationship in lowlanders and natives at high altitude. J Cereb Blood Flow Metab 2013;1-10
28. Sorond FA, Serrador JM, Jones RN, et al. The sit-to-stand technique for the measurement of dynamic cerebral autoregulation. Ultrasound Med Biol 2009;35(1):21-9
29. Reinhard M, Müller T, Guschlbauer B, et al. Transfer function analysis for clinical evaluation of dynamic cerebral autoregulation-a comparison between spontaneous and respiratory-induced oscillations. Physiol Meas 2003;24(1):27-43
30. Levine B, Giller C, Lane L. Cerebral versus systemic hemodynamics during graded orthostatic stress in humans. Circulation 1994;90(1):298-306
31. Tiecks FP, Douville C, Byrd S, et al. Evaluation of impaired cerebral autoregulation by the Valsalva maneuver. Stroke 1996;27:1177-82
32. Smielewski P, Czosnyka M, Kirkpatrick P, Pickard JD. Evaluation of the transient hyperemic response test in head-injured patients. J Neurosurg 1997;86(5):773-8
33. Tibble RK, Girling KJ, Mahajan RP. A comparison of the transient hyperemic response test and the static autoregulation test to assess graded impairment in cerebral autoregulation during propofol, desflurane, and nitrous oxide anesthesia. Anesth Analg 2001;93(1):171-6
34. Panerai RB. Cerebral autoregulation: from models to clinical applications. Cardiovasc Eng 2008;8(1):42-59
35. Czosnyka M, Smielewski P, Kirkpatrick P, et al. Monitoring of cerebral autoregulation in head-injured patients. Stroke 1996;27:1829-34
36. Czosnyka M, Smielewski P, Piechnik S, et al. Cerebral autoregulation following head injury. J Neurosurg 2001;95(5):756-63
37. Calamante F, Thomas DL, Pell GS, et al. Measuring cerebral blood flow using magnetic resonance imaging techniques. J Cereb blood flow Metab 1999;19:701-35
38. Ye F, Berman K, Ellmore T, et al. H(2)(15) O PET validation of steady-state arterial spin tagging cerebral blood flow measurements in humans. Magn Reson Med 2000;44(3):450-6
39. Oktar SO, Yücel C, Karaosmanoglu D, et al. Blood-flow volume quantification in internal carotid and vertebral arteries: comparison of 3 different ultrasound techniques with phase-contrast MR imaging. AJNR Am J Neuroradiol 2006;27(2):363-9
40. Ainslie PN, Hoiland RL. Transcranial Doppler Ultrasound: Valid, Invalid, or Both? J Appl Physiol 2014;1-10
41. Rosenthal G, Sanchez-Mejia RO, Phan N, et al. Incorporating a parenchymal thermal diffusion cerebral blood flow probe in bedside assessment of cerebral autoregulation and vasoreactivity in patients with severe traumatic brain injury. J Neurosurg 2011;114(1):62-70
42. Kirkpatrick PJ, Smielewski P, Czosnyka M, Pickard JD. Continuous monitoring of cortical perfusion by laser Doppler flowmetry in ventilated patients with head injury. J Neurol Neurosurg Psychiatry 1994;57(11):1382-8
43. Brady K, Joshi B, Zweifel C, et al. Real-time continuous monitoring of cerebral blood flow autoregulation using near-infrared spectroscopy in patients undergoing cardiopulmonary bypass. Stroke 2010;41(9):1951-6
44. Mitra S, Czosnyka M, Smielewski P, et al. Heart rate passivity of cerebral tissue oxygenation is associated with predictors of poor outcome in preterm infants. Acta Paediatr 2014;1-9
45. Budohoski K, Czosnyka M, Smielewski P, et al. Impairment of cerebral autoregulation predicts delayed cerebral ischemia after subarachnoid hemorrhage: a prospective observational study. Stroke 2012;43(12):3230-7
46. Zweifel C, Castellani G, Czosnyka M, et al. Noninvasive monitoring of cerebrovascular reactivity with near infrared spectroscopy in head-injured patients. J Neurotrauma 2010;27:1951-8
47. Diedler J, Zweifel C, Budohoski KP, et al. The limitations of near-infrared spectroscopy to assess cerebrovascular reactivity: the role of slow frequency oscillations. Anesth Analg 2011;113(4):849-57
48. Gobiet W, Grote W, Bock WJ. The relation between intracrainal pressure, mean arterial pressure and cerebral blood flow in patients with severe head injury. Acta Neurochir (Wien) 1975;32(1-2):13-24
49. Czosnyka M, Smielewski P, Kirkpatrick P, et al. Continuous assessment of the cerebral vasomotor reactivity in head injury. Neurosurgery 1997;41:11-17. discussion 17-19
50. Nordström C-H, Nielsen TH. Critical thresholds for cerebrovascular reactivity: fact or fiction? Neurocrit Care 2012;17(1):150-1 .author reply 152-3
51. Nordström C-H, Nielsen TH. Continuous determination of optimal cerebral perfusion pressure - in search of the holy grail? Crit Care Med 2013;41(1):e3-4
52. Brady KM, Lee JK, Kibler KK, et al. Continuous measurement of autoregulation by spontaneous fluctuations in cerebral perfusion pressure: comparison of 3 methods. Stroke 2008;39(9):2531-7.
53. Steiner LA, Czosnyka M, Piechnik SK, et al. Continuous monitoring of cerebrovascular pressure reactivity allows determination of optimal cerebral perfusion pressure in patients with traumatic brain injury. Crit Care Med 2002;30(4):733-8.
54. Aries MJH, Czosnyka M, Budohoski KP, et al. Continuous determination of optimal cerebral perfusion pressure in traumatic brain injury. Crit Care Med 2012;40(8):2456-63
55. Zweifel C, Dias C, Smielewski P, Czosnyka M. Continuous time-domain monitoring of cerebral autoregulation in neurocritical care. Med Eng Phys 2014;36(5):638-45
56. Paulson OB, Strandgaard S, Edvinsson L. Cerebral autoregulation. Cerebrovasc Brain Metab Rev 1990;2(2):161-92
57. Koller A, Toth P. Contribution of flow-dependent vasomotor mechanisms to the autoregulation of cerebral blood flow. J Vasc Res 2012;49(5):375-89
58. Engelborghs K, Haseldonckx M, Van Reempts J, et al. Impaired autoregulation of cerebral blood flow in an experimental model of traumatic brain injury. J Neurotrauma 2000;17:667-77
59. Panerai RB, Kerins V, Fan L, et al. Association between dynamic cerebral autoregulation and mortality in severe head injury. Br J Neurosurg 2004;18:471-9
60. Budohoski KP, Czosnyka M, Kirkpatrick PJ, et al. Clinical relevance of cerebral autoregulation following subarachnoid haemorrhage. Nat Rev Neurol 2013;9(3):152-63
61. Jaeger M, Schuhmann MU, Soehle M, et al. Continuous monitoring of cerebrovascular autoregulation after subarachnoid hemorrhage by brain tissue oxygen pressure reactivity and its relation to delayed cerebral infarction. Stroke 2007;38(3):981-6
62. Budohoski K, Czosnyka M. Bilateral failure of cerebral autoregulation is related to unfavorable outcome after subarachnoid hemorrhage. Neurocrit Care 2014. [Epub ahead of print]
63. Lang EW, Diehl RR, Mehdorn HM. Cerebral autoregulation testing after aneurysmal subarachnoid hemorrhage: the phase relationship between arterial blood pressure and cerebral blood flow velocity. Crit Care Med 2001;29(1):158-63
64. McGirt MJ, Lynch JR, Parra A, et al. Simvastatin increases endothelial nitric oxide synthase and ameliorates cerebral vasospasm resulting from subarachnoid hemorrhage. Stroke 2002;33(12):2950-6
65. Tseng M-Y, Czosnyka M, Richards H, et al. Effects of acute treatment with pravastatin on cerebral vasospasm, autoregulation, and delayed ischemic deficits after aneurysmal subarachnoid hemorrhage: a phase II randomized placebo-controlled trial. Stroke 2005;36(8):1627-32
66. Kirkpatrick PJ, Turner CL, Smith C, et al. Simvastatin in aneurysmal subarachnoid haemorrhage (STASH): a multicentre randomised phase 3 trial. Lancet Neurol 2014;13(7):666-75
67. Eames PJ, Blake MJ, Dawson SL, et al. Dynamic cerebral autoregulation and beat to beat blood pressure control are impaired in acute ischaemic stroke. J Neurol Neurosurg Psychiatry 2002;72(4):467-72
68. Reinhard M, Roth M, Guschlbauer B, et al. Dynamic cerebral autoregulation in acute ischemic stroke assessed from spontaneous blood pressure fluctuations. Stroke 2005;36(8):1684-9
69. Immink R V, van Montfrans GA, Stam J, et al. Dynamic cerebral autoregulation in acute lacunar and middle cerebral artery territory ischemic stroke. Stroke 2005;36(12):2595-600
70. Kwan J, Lunt M, Jenkinson D. Assessing dynamic cerebral autoregulation after stroke using a novel technique of combining transcranial Doppler ultrasonography and rhythmic handgrip. Blood Press Monit 2004;9(1):3-8
71. Reinhard M, Rutsch S, Lambeck J, et al. Dynamic cerebral autoregulation associates with infarct size and outcome after ischemic stroke. Acta Neurol Scand 2012;125(3):156-62
72. Ringelstein E, Sievers C, Ecker S. Noninvasive assessment of CO2-induced cerebral vasomotor response in normal individuals and patients with internal carotid artery occlusions. Stroke 1988;19(8):963-9
73. Reinhard M, Gerds TA, Grabiak D, et al. Cerebral dysautoregulation and the risk of ischemic events in occlusive carotid artery disease. J Neurol 2008;255(8):1182-9
74. Reinhard M, Roth M, Müller T, et al. Effect of carotid endarterectomy or stenting on impairment of dynamic cerebral autoregulation. Stroke 2004;35(6):1381-7
75. Obrig H. NeuroImage NIRS in clinical neurology - a promising tool ? Neuroimage 2014;85:535-46
76. Brew N, Walker D, Wong FY. Cerebral vascular regulation and brain injury in preterm infants. Am J Physiol Regul Integr Comp Physiol 2014;306(11):R773-86
77. Lou HC, Lassen NA, Friis-Hansen B. Impaired autoregulation of cerebral blood flow in the distressed newborn infant. J Pediatr 1979;94(1):118-21
78. Rhee CJ, Fraser Iii CD, Kibler K, et al. The ontogeny of cerebrovascular pressure autoregulation in premature infants. J Perinatol 2014;1-6
79. Zhang Y, Chan GSH, Tracy MB, et al. Spectral analysis of systemic and cerebral cardiovascular variabilities in preterm infants: relationship with clinical risk index for babies (CRIB). Physiol Meas 2011;32(12):1913-28
80. Wong FY, Leung TS, Austin T, et al. Impaired autoregulation in preterm infants identified by using spatially resolved spectroscopy. Pediatrics 2008;121:e604-11
81. Greisen G. Autoregulation of cerebral blood flow in newborn babies. Early Hum Dev 2005;81(5):423-8
82. Vutskits L. Cerebral blood flow in the neonate. Paediatr Anaesth 2014;24(1):22-9
83. Bradley WG. Normal pressure hydrocephalus: new concepts on etiology and diagnosis. AJNR Am J Neuroradiol 2000;21(40):1586-90
84. Kristensen B, Malm J, Fagerland M, et al. Regional cerebral blood flow, white matter abnormalities, and cerebrospinal fluid hydrodynamics in patients with idiopathic adult hydrocephalus syndrome. J Neurol Neurosurg Psychiatry 1996;60(3):282-8
85. Owler BK, Momjian S, Czosnyka Z, et al. Normal pressure hydrocephalus and cerebral blood flow: a PET study of baseline values. J Cereb Blood Flow Metab 2004;24:17-23
86. Momjian S, Owler BK, Czosnyka Z, et al. Pattern of white matter regional cerebral blood flow and autoregulation in normal pressure hydrocephalus. Brain 2004;127(Pt 5):965-72
87. Czosnyka Z, van den Boogaard F, Czosnyka M, et al. The relationship between CSF circulation and cerebrovascular pressure-reactivity in normal pressure hydrocephalus. Acta Neurochir Suppl 2005;95:207-11
88. Hogue CW Jr, Palin CA, Arrowsmith JE. Cardiopulmonary bypass management and neurologic outcomes: an evidence-based appraisal of current practices. Anesth Analg 2006;103:21-37
89. Ono M, Joshi B, Brady K, et al. Risks for impaired cerebral autoregulation during cardiopulmonary bypass and postoperative stroke. Br J Anaesth 2012;109:391-8
90. Ono M, Arnaoutakis GJ, Fine DM, et al. Blood pressure excursions below the cerebral autoregulation threshold during cardiac surgery are associated with acute kidney injury. Crit Care Med 2013;41(2):464-71
91. Czosnyka M, Hutchinson PJ, Balestreri M, et al. Monitoring and interpretation of intracranial pressure after head injury. Acta Neurochir Suppl 2006;96:114-18
92. Hauerberg J, Juhler M, Rasmussen G. Cerebral blood flow autoregulation after experimental subarachnoid hemorrhage during hyperventilation in rats. J Neurosurg Anesthesiol 1993;5:258-63
93. Kety SS, Schmidt CF. The effects of altered arterial tensions of carbon dioxide and oxygen on cerebral blood flow and cerebral oxygen consumption of normal young men. J Clin Invest 1948;27:484-92
94. Schneider GH, Sarrafzadeh AS, Kiening KL, et al. Influence of hyperventilation on brain tissue-PO2, PCO2, and pH in patients with intracranial hypertension. Acta Neurochir Suppl 1998;71:62-5
95. Muizelaar JP, Marmarou A, Ward JD, et al. Adverse effects of prolonged hyperventilation in patients with severe head injury: a randomized clinical trial. J Neurosurg 1991;75:731-9
96. Muizelaar JP, van der PH, Li ZC, et al. Pial arteriolar vessel diameter and CO2 reactivity during prolonged hyperventilation in the rabbit. J Neurosurg 1988;69:923-7
97. Mahfoud F, Beck J, Raabe A. Intracranial pressure pulse amplitude during changes in head elevation: a new parameter for determining optimum cerebral perfusion pressure? Acta Neurochir (Wien) 2010;152(3):443-50
98. Feldman Z, Kanter MJ, Robertson CS, et al. Effect of head elevation on intracranial pressure, cerebral perfusion pressure, and cerebral blood flow in head-injured patients. J Neurosurg 1992;76:207-11
99. Jauch E, Saver J, Adams H. Management of patients with acute ischemic stroke a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke 2013;44(3):870-947
100. Wang H, Lynch JR, Song P, et al. Simvastatin and atorvastatin improve behavioral outcome, reduce hippocampal degeneration, and improve cerebral blood flow after experimental traumatic brain injury. Exp Neurol 2007;206(1):59-69
101. Springborg JB, Ma X, Rochat P, et al. A single subcutaneous bolus of erythropoietin normalizes cerebral blood flow autoregulation after subarachnoid haemorrhage in rats. Br J Pharmacol 2002;135(3):823-9
102. Tseng M-Y, Hutchinson PJ, Richards HK, et al. Acute systemic erythropoietin therapy to reduce delayed ischemic deficits following aneurysmal subarachnoid hemorrhage: a Phase II randomized, double-blind, placebo-controlled trial. Clinical article. J Neurosurg 2009;111(1):171-80
103. Rasmussen P, Kim Y-S, Krogh-Madsen R, et al. Both acute and prolonged administration of EPO reduce cerebral and systemic vascular conductance in humans. FASEB J 2012;26(3):1343-8
104. Ehrenreich H, Weissenborn K, Prange H, et al. Recombinant human erythropoietin in the treatment of acute ischemic stroke. Stroke 2009;40:e647-56
105. Renic M, Klaus JA, Omura T, et al. Effect of 20-HETE inhibition on infarct volume and cerebral blood flow after transient middle cerebral artery occlusion. J Cereb Blood Flow Metab 2009;29(3):629-39
106. Strandgaard S, Paulson OB. Antihypertensive drugs and cerebral circulation. Eur J Clin Invest 1996;26(8):625-30
107. Takada J, Ibayashi S, Ooboshi H, et al. Valsartan improves the lower limit of cerebral autoregulation in rats. Hypertens Res 2006;29(8):621-6
108. Näveri L, Strömberg C, Saavedra JM. Angiotensin II AT2 receptor stimulation increases cerebrovascular resistance during hemorrhagic hypotension in rats. Regul Pept 1994;52:21-9
109. Takada J, Ibayashi S, Nagao T, et al. Bradykinin mediates the acute effect of an angiotensin-converting enzyme inhibitor on cerebral autoregulation in rats. Stroke 2001; 32(5):1216-19
110. Waldemar G, Schmidt JF, Andersen AR, et al. Angiotensin converting enzyme inhibition and cerebral blood flow autoregulation in normotensive and hypertensive man. J Hypertens 1989;7:229-35
111. Meel-van den Abeelen ASS, Simpson DM, Wang LJY, et al. Between-centre variability in transfer function analysis, a widely used method for linear quantification of the dynamic pressure-flow relation: the CARNet study. Med Eng Phys 2014;36(5):620-7
112. Czosnyka M, Smielewski P, Piechnik S, et al. Hemodynamic characterization of intracranial pressure plateau waves in head-injury patients. J Neurosurg 1999;91(1):11-19