Measuring cerebrovascular reactivity: What stimulus to use?

Journal of Physiology

Volumn 591, Issue 23, 2013, Pages 5809-5821

  Fierstra, J ^a   Sobczyk, O ^b   Battisti Charbonney, A ^c   Mandell, D M ^c   Poublanc, J ^c   Crawley, A P ^c   Mikulis, D J ^c   Duffin, J ^c   Fisher, J A ^c  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ACETAZOLAMIDE; CARBON DIOXIDE;

BLOOD PRESSURE MEASUREMENT; BLOOD VESSEL REACTIVITY; BRAIN BLOOD FLOW; BREATH HOLDING; CARBON DIOXIDE BREATHING; CEREBROVASCULAR REACTIVITY; CHEMICAL STRESS; DYNAMIC END TIDAL FORCING; HUMAN; HYPERCAPNIA; HYPOTENSION; INVESTIGATIVE PROCEDURES; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROSPECTIVE END TIDAL TARGETING; REBREATHING; REVIEW; VASODILATATION;

BRAIN; CEREBROVASCULAR CIRCULATION; HUMANS; HYPERCAPNIA; VASODILATION;

EID: 84888434437     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2013.259150     Document Type: Review

References (107)

1. Aaslid R, Lindegaard KF, Sorteberg W & Nornes H (1989). Cerebral autoregulation dynamics in humans. Stroke 20, 45-52.
2. 2 reactivity and chemoreflex control of breathing: mechanisms of regulation, measurement, and interpretation. Am J Physiol Regul Integr Comp Physiol 296, R1473-R1495.
3. Alderliesten T, De Vis JB, Lemmers PM, Van Bel F, Benders MJ, Hendrikse J & Petersen ET (2013). Simultaneous quantitative assessment of cerebral physiology using respiratory-calibrated MRI and near-infrared spectroscopy in healthy adults. Neuroimage (in press; DOI: 10.1016/j.neuroimage.2013.07.015).
4. Artru a A & Colley PS (1984). Cerebral blood flow responses to hypocapnia during hypotension. Stroke 15, 878-883.
5. Asghar MS, Hansen a E, Pedersen S, Larsson HB & Ashina M (2011). Pharmacological modulation of the BOLD response: a study of acetazolamide and glyceryl trinitrate in humans. J Magn Reson Imaging 34, 921-927.
6. Attwell D, Buchan a M, Charpak S, Lauritzen M, MacVicar BA & Newman EA (2011). Glial and neuronal control of brain blood flow. Nature 468, 232-243.
7. Ayas N, Bergstrom LR, Schwab TR & Narr BJ (1998). Unrecognized severe postoperative hypercapnia: a case of apneic oxygenation. Mayo Clin Proc 73, 51-54.
8. Baddeley H, Brodrick P M, Taylor NJ, Abdelatti MO, Jordan LC, Vasudevan a S, Phillips H, Saunders MI & Hoskin PJ (2000). Gas exchange parameters in radiotherapy patients during breathing of 2%, 3.5% and 5% carbogen gas mixtures. Br J Radiol 73, 1100-1104.
9. Badgwell JM, Mcleod ME, Lerman J & Creighton RE (1987). End-tidal P measurements sampled at the distal and proximal ends of the endotracheal tube in infants and children. Anesth Analg 66, 959-964.
10. Barr PO (1963). Pulmonary gas exchange in man as affected by prolonged gravitational stress. Acta Psychiatr Scand Suppl 207, 1-46.
11. Battisti-Charbonney A, Fisher J & Duffin J (2011). The cerebrovascular response to carbon dioxide in humans. J Physiol 589, 3039-3048.
12. Beaudin AE, Brugniaux JV, Vohringer M, Flewitt J, Green JD, Friedrich MG & Poulin MJ (2011). Cerebral and myocardial blood flow responses to hypercapnia and hypoxia in humans. Am J Physiol Heart Circ Physiol 301, H1678-H1686.
13. Bishop CC, Butler L, Hunt T, Burnand KG & Browse NL (1987). Effect of carotid endarterectomy on cerebral blood flow and its response to hypercapnia. Br J Surg 74, 994-996.
14. Blockley NP, Driver ID, Francis ST, Fisher JA & Gowland PA (2011). An improved method for acquiring cerebrovascular reactivity maps. Magn Reson Med 65, 1278-1286.
15. Brian JE Jr (1998). Carbon dioxide and the cerebral circulation. Anesthesiology 88, 1365-1386.
16. Bright MG, Bulte DP, Jezzard P & Duyn JH (2009). Characterization of regional heterogeneity in cerebrovascular reactivity dynamics using novel hypocapnia task and BOLD fMRI. Neuroimage 48, 166-175.
17. Bright MG & Murphy K (2013). Reliable quantification of BOLD fMRI cerebrovascular reactivity despite poor breath-hold performance. Neuroimage 83C, 559-568.
18. Casey K, Duffin J & McAvoy GV (1987). The effect of exercise on the central-chemoreceptor threshold in man. J Physiol 383, 9-18.
19. Claassen JA, Zhang R, Fu Q, Witkowski S & Levine BD (2007). Transcranial Doppler estimation of cerebral blood flow and cerebrovascular conductance during modified rebreathing. J Appl Physiol 102, 870-877.
20. Dahl A, Russell D, Rootwelt K, Nyberg-Hansen R & Kerty E (1995). Cerebral vasoreactivity assessed with transcranial Doppler and regional cerebral blood flow measurements. Dose, serum concentration, and time course of the response to acetazolamide. Stroke 26, 2302-2306.
21. Duffin J (2011). Measuring the respiratory chemoreflexes in humans. Resp Physiol Neurobiol 177, 71-79.
22. 2. J Physiol 588, 539-549.
23. Feihl F & Perret C (1994). Permissive hypercapnia. How permissive should we be Am J Respir Crit Care Med 150, 1722-1737.
24. 2 gradient in mechanically ventilated pigs. Intensive Care Med 37, 1543-1550.
25. Floyd TF, Clark JM, Gelfand R, Detre JA, Ratcliffe S, Guvakov D, Lambertsen CJ & Eckenhoff RG (2003). Independent cerebral vasoconstrictive effects of hyperoxia and accompanying arterial hypocapnia at 1 ATA. J Appl Physiol 95, 2453-2461.
26. Fortune JB, Bock D, Kupinski AM, Stratton HH & Shah DM (1992). Human cerebrovascular response to oxygen and carbon dioxide as determined by internal carotid artery duplex scanning. J Trauma 32, 618-627 (Discussion pp. 627-618).
27. Glodzik L, Rusinek H, Brys M, Tsui WH, Switalski R, Mosconi L, Mistur R, Pirraglia E, De Santi S, Li Y, Goldowsky A & De Leon MJ (2011). Framingham cardiovascular risk profile correlates with impaired hippocampal and cortical vasoreactivity to hypercapnia. J Cereb Blood Flow Metab 31, 671-679.
28. 2 reactivity and asymmetry of haemodynamic parameters in patients with carotid artery stenotic disease. A clinical appraisal. Acta Neurochir (Wien) 145, 527-532.
29. Grenier B, Verchere E, Mesli A, Dubreuil M, Siao D, Vandendriessche M, Cales J & Maurette P (1999). Capnography monitoring during neurosurgery: reliability in relation to various intraoperative positions. Anesth Analg 88, 43-48.
30. Grossmann WM & Koeberle B (2000). The dose-response relationship of acetazolamide on the cerebral blood flow in normal subjects. Cerebrovasc Dis 10, 65-69.
31. Gur AY, Bova I & Bornstein NM (1996). Is impaired cerebral vasomotor reactivity a predictive factor of stroke in asymptomatic patients Stroke 27, 2188-2190.
32. Hajjar I, Zhao P, Alsop D & Novak V (2010). Hypertension and cerebral vasoreactivity: a continuous arterial spin labelling magnetic resonance imaging study. Hypertension 56, 859-864.
33. Harper AM (1965). The inter-relationship between aPco-2 and blood pressure in the regulation of blood flow through the cerebral cortex. Acta Neurol Scand Suppl 14, 94-103.
34. Hasegawa Y & Yamaguchi T (1993). [Long-term prognosis and blood flow reactivity to acetazolamide in atherothrombotic brain ischemia]. Rinsho Shinkeigaku 33, 169-174.
35. Hoge RD, Atkinson J, Gill B, Crelier GR, Marrett S & Pike GB (1999). Stimulus-dependent BOLD and perfusion dynamics in human V1. Neuroimage 9, 573-585.
36. Hoskins PR (1990). Measurement of arterial blood flow by Doppler ultrasound. Clin Phys Physiol Meas 11, 1-26.
37. Iadecola C & Nedergaard M (2007). Glial regulation of the cerebral microvasculature. Nat Neurosci 10, 1369-1376.
38. CO2 in subjects at rest. J Physiol 586, 3675-3682.
39. Jensen D, Mask G & Tschakovsky ME (2010). Variability of the ventilatory response to Duffin's modified hyperoxic and hypoxic rebreathing procedure in healthy awake humans. Respir Physiol Neurobiol 170, 185-197.
40. CO2 in exercise. J Appl Physiol 47, 954-960.
41. Kastrup A, Kruger G, Glover GH, Neumann-Haefelin T & Moseley ME (1999). Regional variability of cerebral blood oxygenation response to hypercapnia. Neuroimage 10, 675-681.
42. 2 and breath holding. Magn Reson Imaging 19, 13-20.
43. Kety SS & Schmidt CF (1948). The effects of altered arterial tension of carbon dioxide and oxygen on cerebral blood flow and cerebral oxygen consumption of normal men. J Clin Invest 27, 484-492.
44. Kuroda S, Houkin K, Kamiyama H, Mitsumori K, Iwasaki Y & Abe H (2001). Long-term prognosis of medically treated patients with internal carotid or middle cerebral artery occlusion: can acetazolamide test predict it Stroke 32, 2110-2116.
45. Lee JY & Lee YS (2011). Vasomotor reactivity in middle cerebral artery stenosis. J Neurol Sci 301, 35-37.
46. CO2 gradient during exercise in normal subjects and in patients with severe COPD. Chest 107, 1218-1224.
47. Lucas SJ, Tzeng YC, Galvin SD, Thomas KN, Ogoh S & Ainslie PN (2010). Influence of changes in blood pressure on cerebral perfusion and oxygenation. Hypertension 55, 698-705.
48. Lundar T, Lindegaard KF, Froysaker T, Aaslid R, Grip A & Nornes H (1985). Dissociation between cerebral autoregulation and carbon dioxide reactivity during nonpulsatile cardiopulmonary bypass. Ann Thorac Surg 40, 582-587.
49. 2 and Paco2 in children receiving mechanical ventilation. Pediatr Crit Care Med 3, 244-249.
50. MacKenzie ET, Farrar JK, Fitch W, Graham DI, Gregory PC & Harper a M (1979). Effects of hemorrhagic hypotension on the cerebral circulation. I. Cerebral blood flow and pial arteriolar caliber. Stroke 10, 711-718.
51. Mahony PJ, Panerai RB, Deverson ST, Hayes PD & Evans DH (2000). Assessment of the thigh cuff technique for measurement of dynamic cerebral autoregulation. Stroke 31, 476-480.
52. Mandell DM, Han JS, Poublanc J, Crawley AP, Fierstra J, Tymianski M, Fisher JA & Mikulis DJ (2011). Quantitative measurement of cerebrovascular reactivity by blood oxygen level-dependent MR imaging in patients with intracranial stenosis: preoperative cerebrovascular reactivity predicts the effect of extracranial-intracranial bypass surgery. AJNR Am J Neuroradiol 32, 721-727.
53. Mandell DM, Han JS, Poublanc J, Crawley AP, Stainsby JA, Fisher JA & Mikulis DJ (2008). Mapping cerebrovascular reactivity using blood oxygen level-dependent MRI in Patients with arterial steno-occlusive disease: comparison with arterial spin labelling MRI. Stroke 39, 2021-2028.
54. Mardimae A, Balaban DY, Machina MA, Han JS, Katznelson R, Minkovich LL, Fedorko L, Murphy PM, Wasowicz M, Naughton F, Meineri M, Fisher JA & Duffin J (2012). The interaction of carbon dioxide and hypoxia in the control of cerebral blood flow. Pflugers Arch 464, 345-351.
55. Mark CI, Fisher JA & Pike GB (2011). Improved fMRI calibration: precisely controlled hyperoxic versus hypercapnic stimuli. Neuroimage 54, 1102-1111.
56. Mark CI, Slessarev M, Ito S, Han J, Fisher JA & Pike GB (2010). Precise control of end-tidal carbon dioxide and oxygen improves BOLD and ASL cerebrovascular reactivity measures. Magn Reson Med 64, 749-756.
57. Markus HS & Harrison MJ (1992). Estimation of cerebrovascular reactivity using transcranial Doppler, including the use of breath-holding as the vasodilatory stimulus. Stroke 23, 668-673.
58. Miller RM & Tenney SM (1956). Dead space ventilation in old age. J Appl Physiol 9, 321-327.
59. Murphy K, Harris a D & Wise RG (2011). Robustly measuring vascular reactivity differences with breath-hold: normalising stimulus-evoked and resting state BOLD fMRI data. Neuroimage 54, 369-379.
60. 2 inhalation in patients with major cerebral artery occlusive disease: a positron-emission tomography study. Neuroradiology 41, 73-79.
61. O'Croinin D, Ni Chonghaile M, Higgins B & Laffey JG (2005). Bench-to-bedside review: Permissive hypercapnia. Crit Care 9, 51-59.
62. Okazawa H, Yamauchi H, Sugimoto K, Toyoda H, Kishibe Y & Takahashi M (2001). Effects of acetazolamide on cerebral blood flow, blood volume, and oxygen metabolism: a positron emission tomography study with healthy volunteers. J Cereb Blood Flow Metab 21, 1472-1479.
63. Panerai RB (1998). Assessment of cerebral pressure autoregulation in humans - a review of measurement methods. Physiol Meas 19, 305-338.
64. Paulson OB, Hasselbalch SG, Rostrup E, Knudsen GM & Pelligrino D (2011). Cerebral blood flow response to functional activation. J Cereb Blood Flow Metab 30, 2-14.
65. Potkin RT & Swenson ER (1992). Resuscitation from severe acute hypercapnia. Determinants of tolerance and survival. Chest 102, 1742-1745.
66. Poulin MJ, Fatemian M, Tansley JG, O'Connor DF & Robbins PA (2002). Changes in cerebral blood flow during and after 48 h of both isocapnic and poikilocapnic hypoxia in humans. Exp Physiol 87, 633-642.
67. CO2 in humans. J Appl Physiol 81, 1084-1095.
68. 2 in emergency patients. Resuscitation 35, 145-148.
69. 2 on blood oxygen level-dependent (BOLD) MRI. J Magn Reson Imaging 27, 185-191.
70. Raichle ME & Plum F (1972). Hyperventilation and cerebral blood flow. Stroke 3, 566-575.
71. Ratnatunga C & Adiseshiah M (1990). Increase in middle cerebral artery velocity on breath holding: a simplified test of cerebral perfusion reserve. Eur J Vasc Surg 4, 519-523.
72. Read DJ (1967). A clinical method for assessing the ventilatory response to carbon dioxide. Australas Ann Med 16, 20-32.
73. 2-induced cerebral vasomotor response in normal individuals and patients with internal carotid artery occlusions. Stroke 19, 963-969.
74. 2 to acetazolamide. J Cereb Blood Flow Metab 12, 162-168.
75. CO2 in men. J Appl Physiol 68, 1727-1731.
76. Robbins PA, Swanson GD & Howson MG (1982a). A prediction-correction scheme for forcing alveolar gases along certain time courses. J Appl Physiol 52, 1353-1357.
77. Robbins PA, Swanson GD, Micco AJ & Schubert WP (1982b). A fast gas-mixing system for breath-to-breath respiratory control studies. J Appl Physiol 52, 1358-1362.
78. Russell GB & Graybeal JM (1994). Reliability of the arterial to end-tidal carbon dioxide gradient in mechanically ventilated patients with multisystem trauma. J Trauma 36, 317-322.
79. Russo G, Lodi CA & Ursino M (2000). Quantitative assessment of cerebral vascular reserve by means of transcranial Doppler ultrasound and rebreathing maneuver: bedside test and mathematical modelling. Neurol Sci 21, 292-302.
80. CO2 in the elderly. J Appl Physiol 79, 2086-2093.
81. Saito H, Ogasawara K, Suzuki T, Kuroda H, Kobayashi M, Yoshida K, Kubo Y & Ogawa A (2011). Adverse effects of intravenous acetazolamide administration for evaluation of cerebrovascular reactivity using brain perfusion single-photon emission computed tomography in patients with major cerebral artery steno-occlusive diseases. Neurol Med Chir (Tokyo) 51, 479-483.
82. Sasse SA, Berry RB, Nguyen TK, Light RW & Mahutte CK (1996). Arterial blood gas changes during breath-holding from functional residual capacity. Chest 110, 958-964.
83. 2 in human internal and external carotid and vertebral arteries. J Physiol 590, 3277-3290.
84. Scouten A & Schwarzbauer C (2008). Paced respiration with end-expiration technique offers superior BOLD signal repeatability for breath-hold studies. Neuroimage 43, 250-257.
85. Silvestrini M, Vernieri F, Pasqualetti P, Matteis M, Passarelli F, Troisi E & Caltagirone C (2000). Impaired cerebral vasoreactivity and risk of stroke in patients with asymptomatic carotid artery stenosis. JAMA 283, 2122-2127.
86. Silvestrini M, Vernieri F, Troisi E, Passarelli F, Matteis M, Pasqualetti P, Rossini PM & Caltagirone C (1999). Cerebrovascular reactivity in carotid artery occlusion: possible implications for surgical management of selected groups of patients. Acta Neurol Scand 99, 187-191.
87. Skow RJ, Mackay CM, Tymko MM, Willie CK, Smith KJ, Ainslie PN & Day TA (2013). Differential cerebrovascular CO reactivity in anterior and posterior cerebral circulations. Respir Physiol Neurobiol 189, 76-86.
88. 2 concentrations. J Physiol 581, 1207-1219.
89. Sommer LZ, Iscoe S, Robicsek A, Kruger J, Silverman J, Rucker J, Dickstein J, Volgyesi GA & Fisher JA (1998). A simple breathing circuit minimizing changes in alveolar ventilation during hyperpnoea. Eur Respir J 12, 698-701.
90. Somogyi RB, Vesely AE, Preiss D, Prisman E, Volgyesi G, Azami T, Iscoe S, Fisher JA & Sasano H (2005). Precise control of end-tidal carbon dioxide levels using sequential rebreathing circuits. Anaesth Intensive Care 33, 726-732.
91. 2 blood oxygen level-dependent MR mapping of cerebrovascular reserve in a clinical population: Safety, tolerability, and technical feasibility. Radiology 266, 592-598.
92. Steinback CD, Salzer D, Medeiros PJ, Kowalchuk J & Shoemaker JK (2009). Hypercapnic vs. hypoxic control of cardiovascular, cardiovagal, and sympathetic function. Am J Physiol Regul Integr Comp Physiol 296, R402-R410.
93. Steiner LA, Balestreri M, Johnston AJ, Coles JP, Chatfield DA, Pickard JD, Menon DK & Czosnyka M (2005). Effects of moderate hyperventilation on cerebrovascular pressure-reactivity after head injury. Acta Neurochir Suppl 95, 17-20.
94. Stock M, Kontrisova K, Dieckmann K, Bogner J, Poetter R & Georg D (2006). Development and application of a real-time monitoring and feedback system for deep inspiration breath hold based on external marker tracking. Med Phys 33, 2868-2877.
95. 2: methods and implications. J Appl Physiol 39, 377-385.
96. 2 inhalation. Scand J Clin Lab Invest Suppl 102, XIII:A.
97. Symon L (1969). The concept of intracerebral steal. Int Anesthesiol Clin 7, 597-615.
98. Tan CO (2012). Defining the characteristic relationship between arterial pressure and cerebral flow. J Appl Physiol 113, 1194-1200.
99. Totaro R, Marini C, Baldassarre M & Carolei A (1999). Cerebrovascular reactivity evaluated by transcranial Doppler: reproducibility of different methods. Cerebrovasc Dis 9, 142-145.
100. Vernieri F, Pasqualetti P, Passarelli F, Rossini PM & Silvestrini M (1999). Outcome of carotid artery occlusion is predicted by cerebrovascular reactivity. Stroke 30, 593-598.
101. Vernieri F, Tibuzzi F, Pasqualetti P, Rosato N, Passarelli F, Rossini PM & Silvestrini M (2004). Transcranial Doppler and near-infrared spectroscopy can evaluate the hemodynamic effect of carotid artery occlusion. Stroke 35, 64-70.
102. Vorstrup S, Brun B & Lassen NA (1986). Evaluation of the cerebral vasodilatory capacity by the acetazolamide test before EC-IC bypass surgery in patients with occlusion of the internal carotid artery. Stroke 17, 1291-1298.
103. Willie CK, Macleod DB, Shaw a D, Smith KJ, Tzeng YC, Eves ND, Ikeda K, Graham J, Lewis NC, Day TA & Ainslie PN (2012). Regional brain blood flow in man during acute changes in arterial blood gases. J Physiol 590, 3261-3275.
104. Wintermark M, Sesay M, Barbier E, Borbely K, Dillon WP, Eastwood JD, Glenn TC, Grandin CB, Pedraza S, Soustiel JF, Nariai T, Zaharchuk G, Caille JM, Dousset V & Yonas H (2005). Comparative overview of brain perfusion imaging techniques. Stroke 36, e83-e99.
105. Wise RG, Pattinson KT, Bulte DP, Chiarelli PA, Mayhew SD, Balanos GM, O'Connor DF, Pragnell TR, Robbins PA, Tracey I & Jezzard P (2007). Dynamic forcing of end-tidal carbon dioxide and oxygen applied to functional magnetic resonance imaging. J Cereb Blood Flow Metab 27, 1521-1532.
106. 2 difference and dead space/tidal volume ratio in respiratory failure. Chest 92, 832-835.
107. Yonas H, Smith HA, Durham SR, Pentheny SL & Johnson DW (1993). Increased stroke risk predicted by compromised cerebral blood flow reactivity. J Neurosurg 79, 483-489.