Reduced CMRO2 and cerebrovascular reserve in patients with severe intracranial arterial stenosis: A combined multiparametric qBOLD oxygenation and BOLD fMRI study

Multiparametric quantitative blood oxygenation level dependent (mqBOLD) magnetic resonance Imaging (MRI) approach allows mapping tissular oxygen saturation (StO2) and cerebral metabolic rate of oxygen (CMRO2). To identify hemodynamic alteration related to severe intracranial arterial stenosis (SIAS), functional MRI of cerebrovascular reserve (CVR BOLD fMRI) to hypercapnia has been proposed. Diffusion imaging suggests chronic low grade ischemia in patients with impaired CVR. The aim of the present study was to evaluate how oxygen parameters (StO2 and CMRO2), assessed with mqBOLD approach, correlate with CVR in patients (n = 12) with SIAS and without arterial occlusion. The perfusion (dynamic susceptibility contrast), oxygenation, and CVR were compared. The MRI protocol conducted at 3T lasted approximately 1 h. Regions of interest measures on maps were delineated on segmented gray matter (GM) of middle cerebral artery territories. We have shown that decreased CVR is spatially associated with decreased CMRO2 in GM of patients with SIAS. Further, the degree of ipsilateral CVR reduction was well‐correlated with the amplitude of the CMRO2 deficit. The altered CMRO2 suggests the presence of a moderate ischemia explained by both a decrease in perfusion and in CVR. CVR and mqBOLD method may be helpful in the selection of patients with SIAS to advocate for medical therapy or percutaneous transluminal angioplasty‐stenting. Hum Brain Mapp 36:695–706, 2015. © 2014 Wiley Periodicals, Inc.

[1]  S. Sakamoto,et al.  Regional difference in cerebral blood flow and oxidative metabolism in human cortex. , 1996, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[2]  Thomas Christen,et al.  Is T2* enough to assess oxygenation? Quantitative blood oxygen level-dependent analysis in brain tumor. , 2012, Radiology.

[3]  D. Mozaffarian,et al.  Heart disease and stroke statistics--2009 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. , 2009, Circulation.

[4]  Heidi Johansen-Berg,et al.  Visualization of Altered Neurovascular Coupling in Chronic Stroke Patients using Multimodal Functional MRI , 2012, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[5]  B. Rosen,et al.  High resolution measurement of cerebral blood flow using intravascular tracer bolus passages. Part I: Mathematical approach and statistical analysis , 1996, Magnetic resonance in medicine.

[6]  Adrian P. Crawley,et al.  Impact of Extracranial–Intracranial Bypass on Cerebrovascular Reactivity and Clinical Outcome in Patients With Symptomatic Moyamoya Vasculopathy , 2011, Stroke.

[7]  H. A. Smith,et al.  A standardized method for measuring intracranial arterial stenosis. , 2000, AJNR. American journal of neuroradiology.

[8]  Sven Haller,et al.  Reduced cerebrovascular reserve at CO2 BOLD MR imaging is associated with increased risk of periinterventional ischemic lesions during carotid endarterectomy or stent placement: preliminary results. , 2008, Radiology.

[9]  W J Powers,et al.  Importance of hemodynamic factors in the prognosis of symptomatic carotid occlusion. , 1999, JAMA.

[10]  E. Shimosegawa,et al.  Chronic Middle Cerebral Artery Occlusion: A Hemodynamic and Metabolic Study with Positron-Emission Tomography , 2008, American Journal of Neuroradiology.

[11]  Donald Sashin,et al.  Identification of Hemodynamic Compromise by Cerebrovascular Reserve and Oxygen Extraction Fraction in Occlusive Vascular Disease , 2004, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[12]  D. Yablonskiy,et al.  Quantitative BOLD: Mapping of human cerebral deoxygenated blood volume and oxygen extraction fraction: Default state , 2007, Magnetic resonance in medicine.

[13]  H. Woo,et al.  US Multicenter Experience With the Wingspan Stent System for the Treatment of Intracranial Atheromatous Disease: Periprocedural Results , 2007, Stroke.

[14]  Jan Warnking,et al.  Normalization of cerebral vasoreactivity using BOLD MRI after intravascular stenting , 2014, Human brain mapping.

[15]  Terry Jones,et al.  Oxygen metabolism, oxygen extraction and positron emission tomography: Historical perspective and impact on basic and clinical neuroscience , 2012, NeuroImage.

[16]  H. An,et al.  Quantitative measurements of cerebral metabolic rate of oxygen utilization using MRI: a volunteer study , 2001, NMR in biomedicine.

[17]  Roland Bammer,et al.  High‐resolution cerebral blood volume imaging in humans using the blood pool contrast agent ferumoxytol , 2013, Magnetic resonance in medicine.

[18]  Takashi Yoshimoto,et al.  Cerebrovascular Reactivity to Acetazolamide and Outcome in Patients With Symptomatic Internal Carotid or Middle Cerebral Artery Occlusion: A Xenon-133 Single-Photon Emission Computed Tomography Study , 2002, Stroke.

[19]  D J Mikulis,et al.  Quantification of Cerebrovascular Reactivity by Blood Oxygen Level–Dependent MR Imaging and Correlation with Conventional Angiography in Patients with Moyamoya Disease , 2010, American Journal of Neuroradiology.

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

[21]  Matus Straka,et al.  Measuring brain oxygenation in humans using a multiparametric quantitative blood oxygenation level dependent MRI approach , 2012, Magnetic resonance in medicine.

[22]  Y Yonekura,et al.  Altered cerebral energy metabolism in Alzheimer's disease: a PET study. , 1994, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[23]  D Yves von Cramon,et al.  Regional Impairment of Cerebrovascular Reactivity and BOLD Signal in Adults After Stroke , 2005, Stroke.

[24]  Tohru Shiga,et al.  Combination of a Mean Transit Time Measurement with an Acetazolamide Test Increases Predictive Power to Identify Elevated Oxygen Extraction Fraction in Occlusive Carotid Artery Diseases , 2008, Journal of Nuclear Medicine.

[25]  E. Haacke,et al.  Theory of NMR signal behavior in magnetically inhomogeneous tissues: The static dephasing regime , 1994, Magnetic resonance in medicine.

[26]  J. Xiao,et al.  Detecting Misery Perfusion in Unilateral Steno-Occlusive Disease of the Internal Carotid Artery or Middle Cerebral Artery by MR Imaging , 2011, American Journal of Neuroradiology.

[27]  D J Mikulis,et al.  Mapping white matter diffusion and cerebrovascular reactivity in carotid occlusive disease , 2011, Neurology.

[28]  H. Fukuyama,et al.  Significance of increased oxygen extraction fraction in five-year prognosis of major cerebral arterial occlusive diseases. , 1999, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[29]  Frederik Barkhof,et al.  Changes in white matter as determinant of global functional decline in older independent outpatients: three year follow-up of LADIS (leukoaraiosis and disability) study cohort , 2009, BMJ : British Medical Journal.

[30]  Thomas Christen,et al.  Evaluation of a quantitative blood oxygenation level‐dependent (qBOLD) approach to map local blood oxygen saturation , 2010, NMR in biomedicine.

[31]  E Vicaut,et al.  Prospective study of symptomatic atherothrombotic intracranial stenoses , 2006, Neurology.

[32]  J. Le Bas,et al.  Functional imaging of cerebral perfusion. , 2013, Diagnostic and interventional imaging.

[33]  E. Barbier,et al.  Tissue Oxygen Saturation Mapping with Magnetic Resonance Imaging , 2014, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[34]  Weili Lin,et al.  Quantitative Measurements of Cerebral Blood Oxygen Saturation Using Magnetic Resonance Imaging , 2000, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[35]  David J Mikulis,et al.  CO2 blood oxygen level-dependent MR mapping of cerebrovascular reserve in a clinical population: safety, tolerability, and technical feasibility. , 2013, Radiology.

[36]  D. Mozaffarian,et al.  Heart disease and stroke statistics--2009 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. , 2009, Circulation.

[37]  Kiyohiro Houkin,et al.  Long-Term Prognosis of Medically Treated Patients With Internal Carotid or Middle Cerebral Artery Occlusion: Can Acetazolamide Test Predict It? , 2001, Stroke.

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

[39]  H. Yonas,et al.  Stages and thresholds of hemodynamic failure. , 2003, Stroke.

[40]  G N Stewart,et al.  Researches on the Circulation Time in Organs and on the Influences which affect it , 1893, The Journal of physiology.

[41]  J. West Pulmonary Physiology and Pathophysiology: An Integrated, Case-Based Approach , 2001 .

[42]  Bojana Stefanovic,et al.  Venous refocusing for volume estimation: VERVE functional magnetic resonance imaging , 2005, Magnetic resonance in medicine.

[43]  Richard B. Buxton,et al.  A general analysis of calibrated BOLD methodology for measuring CMRO2 responses: Comparison of a new approach with existing methods , 2012, NeuroImage.

[44]  Ralf Deichmann,et al.  T2′ Imaging Within Perfusion-Restricted Tissue in High-Grade Occlusive Carotid Disease , 2012, Stroke.

[45]  B. Rosen,et al.  Tracer arrival timing‐insensitive technique for estimating flow in MR perfusion‐weighted imaging using singular value decomposition with a block‐circulant deconvolution matrix , 2003, Magnetic resonance in medicine.

[46]  David J Mikulis,et al.  Mapping Cerebrovascular Reactivity Using Blood Oxygen Level-Dependent MRI in Patients With Arterial Steno-occlusive Disease: Comparison With Arterial Spin Labeling MRI , 2008, Stroke.

[47]  K. Zierler,et al.  On the theory of the indicator-dilution method for measurement of blood flow and volume. , 1954, Journal of applied physiology.

[48]  Sean I. Savitz,et al.  Stenting versus Aggressive Medical Therapy for Intracranial Arterial Stenosis , 2012 .

[49]  Jan Warnking,et al.  Impaired cerebral vasoreactivity to CO2 in Alzheimer's disease using BOLD fMRI , 2011, NeuroImage.

[50]  J. Bogousslavsky,et al.  Stroke Syndromes: Arterial territories of the human brain , 2001 .

[51]  J. Baron,et al.  Oxygen Imaging by MRI: Can Blood Oxygen Level-Dependent Imaging Depict the Ischemic Penumbra? , 2012, Stroke.

[52]  Peter Jezzard,et al.  Measurement of cerebral blood volume in humans using hyperoxic MRI contrast , 2007, Journal of magnetic resonance imaging : JMRI.

[53]  Thomas Christen,et al.  Quantitative MR estimates of blood oxygenation based on T2*: A numerical study of the impact of model assumptions , 2012, Magnetic resonance in medicine.

[54]  E. Vittinghoff,et al.  How Accurate Is CT Angiography in Evaluating Intracranial Atherosclerotic Disease? , 2008, Stroke.

[55]  Zhen Jiang,et al.  Impaired fMRI activation in patients with primary brain tumors , 2010, NeuroImage.