Variability of cerebral blood volume and oxygen extraction: stages of cerebral haemodynamic impairment revisited.

The presence or degree of haemodynamic impairment due to occlusive cerebrovascular disease is often inferred from measurements of cerebral blood flow (CBF), cerebral blood volume (CBV), oxygen extraction fraction (OEF) and the cerebral rate for oxygen metabolism (CMRO2). However, the relationship of these variables, in particular CBV, to regional cerebral haemodynamics is not clearly established in humans with subacute or chronic disease. In the present study, we investigated the relationship of CBV to OEF, CBF and CMRO2, and to subsequent stroke risk in patients with unilateral carotid artery occlusion, in order to define better the associated haemodynamic and metabolic changes. We reviewed data from 81 patients with symptomatic carotid occlusion enrolled in a prospective study of haemodynamic factors and stroke risk. Measurements of CBV, CBF, OEF and CMRO2 were made on entry using PET. Patients were divided into groups by hemispheric ratios and absolute ipsilateral values of OEF and CBV, based on comparison with normal controls. Haemodynamic and metabolic values, risk factors and stroke risk were compared between groups. Based on hemispheric ratios, 45 patients had increased ipsilateral OEF; CBV was increased in 19 of these 45 patients. No differences in CBF, CMRO2 or clinical risk factors were found between these 19 patients and the remaining 26 patients with increased OEF and normal or reduced CBV. Thirteen ipsilateral strokes occurred during follow-up, and 10 of the 13 occurred in the 19 patients with increased OEF and CBV (log rank P < 0.0001). Thirty-two of the 68 patients with complete quantitative PET data had increased OEF by absolute ipsilateral values. CBV was increased in 20 of the 32 patients. No differences in CBF, CMRO2 or clinical risk factors were found between these 20 patients and the remaining 12 patients with increased OEF and normal CBV. Seven of the nine ipsilateral strokes that occurred in the 68 patients occurred in those 20 patients with increased OEF and increased CBV (log rank P = 0.003). The higher risk of ischaemic stroke in patients with increased OEF and CBV suggests that their degree of haemodynamic compromise is more severe than those with increased OEF and normal CBV. In patients with chronic carotid occlusion and increased OEF, increased CBV may indicate pronounced vasodilation due to exhausted autoregulatory vasodilation. The physiological explanation for the measurement of normal CBV in patients with increased OEF is less certain and may reflect preserved autoregulatory capacity.

[1]  M. Mato,et al.  Antiproliferative Effect and Cell Cycle Modulation by Melatonin on GH3 Cells , 2000, Hormone Research in Paediatrics.

[2]  R Weissleder,et al.  Cerebrovascular dynamics of autoregulation and hypoperfusion. An MRI study of CBF and changes in total and microvascular cerebral blood volume during hemorrhagic hypotension. , 1999, Stroke.

[3]  W J Powers,et al.  Count-based PET method for predicting ischemic stroke in patients with symptomatic carotid arterial occlusion. , 1999, Radiology.

[4]  W J Powers,et al.  Cerebral hemodynamic impairment , 1999, Neurology.

[5]  W J Powers,et al.  Compensatory mechanisms for chronic cerebral hypoperfusion in patients with carotid occlusion. , 1999, Stroke.

[6]  William J. Powers,et al.  Importance of Hemodynamic Factors in the Prognosis of Symptomatic Carotid Occlusion , 1998 .

[7]  J Yoshida,et al.  Neural Activation of the Brain with Hemodynamic Insufficiency , 1998, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[8]  J. Baron,et al.  Evaluation of the ratio of cerebral blood flow to cerebral blood volume as an index of local cerebral perfusion pressure. , 1998, Brain : a journal of neurology.

[9]  W J Powers,et al.  Increased oxygen extraction fraction is associated with prior ischemic events in patients with carotid occlusion. , 1998, Stroke.

[10]  H. Fukuyama,et al.  Cerebral hematocrit decreases with hemodynamic compromise in carotid artery occlusion: a PET study. , 1998, Stroke.

[11]  Y Yonekura,et al.  Evidence of misery perfusion and risk for recurrent stroke in major cerebral arterial occlusive diseases from PET. , 1996, Journal of neurology, neurosurgery, and psychiatry.

[12]  H. Fukuyama,et al.  Crossed Cerebellar Hypoperfusion Indicates the Degree of Uncoupling Between Blood Flow and Metabolism in Major Cerebral Arterial Occlusion , 1994, Stroke.

[13]  B. Widder,et al.  Course of Cerebrovascular Reactivity in Patients With Carotid Artery Occlusions , 1994, Stroke.

[14]  Kazuo Minematsu,et al.  Acetazolamide Reactivity on 123I-IMP Single Photon Emission Computed Tomography in Patients with Major Cerebral Artery Occlusive Disease: Correlation with Positron Emission Tomography Parameters , 1994, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[15]  D F Hanley,et al.  Effects of graded hypotension on cerebral blood flow, blood volume, and mean transit time in dogs. , 1992, The American journal of physiology.

[16]  W. Powers Cerebral hemodynamics in ischemic cerebrovascular disease , 1991, Annals of neurology.

[17]  U Dirnagl,et al.  Autoregulation of Cerebral Blood Flow in Experimental Focal Brain Ischemia , 1990, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[18]  K Wienhard,et al.  Use of PET Methods for Measurement of Cerebral Energy Metabolism and Hemodynamics in Cerebrovascular Disease , 1989, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[19]  B Mazoyer,et al.  Local brain haemodynamics and oxygen metabolism in cerebrovascular disease. Positron emission tomography. , 1989, Brain : a journal of neurology.

[20]  F. Shishido,et al.  Oxygen Extraction Fraction at Maximally Vasodilated Tissue in the Ischemic Brain Estimated from the Regional CO2 Responsiveness Measured by Positron Emission Tomography , 1988, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[21]  M E Raichle,et al.  Brain Blood Volume, Flow, and Oxygen Utilization Measured with 15O Radiotracers and Positron Emission Tomography: Revised Metabolic Computations , 1987, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[22]  M. Raichle,et al.  Cerebral Blood Volume Measured with Inhaled C15O and Positron Emission Tomography , 1987, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[23]  M. Raichle,et al.  The effect of hemodynamically significant carotid artery disease on the hemodynamic status of the cerebral circulation. , 1987, Annals of internal medicine.

[24]  M. Raichle,et al.  Cerebral Blood Flow and Cerebral Metabolic Rate of Oxygen Requirements for Cerebral Function and Viability in Humans , 1985, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[25]  J. Baron,et al.  Effects of extra-intracranial arterial bypass on cerebral blood flow and oxygen metabolism in humans. , 1985, Stroke.

[26]  M. Raichle,et al.  A Stereotactic Method of Anatomical Localization for Positron Emission Tomography , 1985, Journal of computer assisted tomography.

[27]  K. Leenders,et al.  EVALUATION OF CEREBRAL PERFUSION RESERVE IN PATIENTS WITH CAROTID-ARTERY OCCLUSION , 1984, The Lancet.

[28]  M. Mintun,et al.  Brain oxygen utilization measured with O-15 radiotracers and positron emission tomography. , 1984, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[29]  D Comar,et al.  Reversal of Focal "Misery‐Perfusion Syndrome" By Extra‐Intracranial Arterial Bypass in Hemodynamic Cerebral Ischemia: A Case Study with 15O Positron Emission Tomography , 1981, Stroke.

[30]  D. Graham,et al.  Effects of Hemorrhagic Hypotension on the Cerebral Circulation: I. Cerebral Blood Flow and Pial Arteriolar Caliber , 1979, Stroke.

[31]  J. Patterson,et al.  Responses of cerebral arteries and arterioles to acute hypotension and hypertension. , 1978, The American journal of physiology.

[32]  M. Raichle,et al.  Effects of increased intracranial pressure on cerebral blood volume, blood flow, and oxygen utilization in monkeys. , 1975, Journal of neurosurgery.

[33]  M E Phelps,et al.  The Effects of Arterial Blood Pressure on the Regional Cerebral Blood Volume by X‐Ray Fluorescence , 1973, Stroke.

[34]  G. Boysen Cerebral hemodynamics in carotid surgery. , 1973, Acta neurologica Scandinavica. Supplementum.

[35]  A H BECKETT,et al.  FAMILIAL NEUROPATHY AND PRESSURE PALSIES. , 1965, Lancet.

[36]  Rapela Ce,et al.  AUTOREGULATION OF CANINE CEREBRAL BLOOD FLOW. , 1964 .

[37]  L. Mchenry,et al.  CEREBRAL HEMODYNAMICS OF SYNCOPE , 1961, The American journal of the medical sciences.

[38]  S. Kety,et al.  The effects of an acute reduction in blood pressure by means of differential spinal sympathetic block on the cerebral circulation of hypertensive patients. , 1950, The Journal of clinical investigation.

[39]  M. Fog CEREBRAL CIRCULATION: THE REACTION OF THE PIAL ARTERIES TO A FALL IN BLOOD PRESSURE , 1937 .

[40]  H. Wolff,et al.  THE CEREBRAL CIRCULATION , 1936 .

[41]  F. Gibbs,et al.  RELATIONSHIP OF UNCONSCIOUSNESS TO CEREBRAL BLOOD FLOW AND TO ANOXEMIA , 1935 .

[42]  H. S. Forbes,et al.  THE CEREBRAL CIRCULATION: I. OBSERVATION AND MEASUREMENT OF PIAL VESSELS , 1928 .