Noninvasive Assessment of Oxygen Extraction Fraction in Chronic Ischemia Using Quantitative Susceptibility Mapping at 7 Tesla

Background and Purpose— The oxygen extraction fraction (OEF) is an effective metric to evaluate metabolic reserve in chronic ischemia. However, OEF is considered to be accurately measured only when using positron emission tomography (PET). Thus, we investigated whether OEF maps generated by magnetic resonance quantitative susceptibility mapping (QSM) at 7 Tesla enabled detection of OEF changes when compared with those obtained with PET. Methods— Forty-one patients with chronic stenosis/occlusion of the unilateral internal carotid artery or middle cerebral artery were examined using 7 Tesla-MRI and PET scanners. QSM images were obtained from 3-dimensional T2*-weighted images, using a multiple dipole-inversion algorithm. OEF maps were generated based on susceptibility differences between venous structures and brain tissues on QSM images. OEF ratios of the ipsilateral middle cerebral artery territory against the contralateral side were calculated on the QSM-OEF and PET-OEF images, using an anatomic template. Results— The OEF ratio in the middle cerebral artery territory showed significant correlations between QSM-OEF and PET-OEF maps (r=0.69; P<0.001), especially in patients with a substantial increase in the PET-OEF ratio of 1.09 (r=0.79; P=0.004), although showing significant systematic biases for the agreements. An increased QSM-OEF ratio of >1.09, as determined by receiver operating characteristic analysis, showed a sensitivity and specificity of 0.82 and 0.86, respectively, for the substantial increase in the PET-OEF ratio. Absolute QSM-OEF values were significantly correlated with PET-OEF values in the patients with increased PET-OEF. Conclusions— OEF ratios on QSM-OEF images at 7 Tesla showed a good correlation with those on PET-OEF images in patients with unilateral steno-occlusive internal carotid artery/middle cerebral artery lesions, suggesting that noninvasive OEF measurement by MRI can be a substitute for PET.

[1]  E Adalsteinsson,et al.  QUantitative Imaging of eXtraction of oxygen and TIssue consumption (QUIXOTIC) using venular‐targeted velocity‐selective spin labeling , 2011, Magnetic resonance in medicine.

[2]  Hanzhang Lu,et al.  Quantitative evaluation of oxygenation in venous vessels using T2‐Relaxation‐Under‐Spin‐Tagging MRI , 2008, Magnetic resonance in medicine.

[3]  Yoshiharu Yonekura,et al.  Cerebral blood flow SPET in transient global amnesia with automated ROI analysis by 3DSRT , 2004, European Journal of Nuclear Medicine and Molecular Imaging.

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

[5]  R. Weisskoff,et al.  MRI susceptometry: Image‐based measurement of absolute susceptibility of MR contrast agents and human blood , 1992, Magnetic resonance in medicine.

[6]  Elfar Adalsteinsson,et al.  Quantitative Oxygen Extraction Fraction from 7-Tesla MRI Phase: Reproducibility and Application in Multiple Sclerosis , 2015, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[7]  Yi Wang,et al.  Calculation of susceptibility through multiple orientation sampling (COSMOS): A method for conditioning the inverse problem from measured magnetic field map to susceptibility source image in MRI , 2009, Magnetic resonance in medicine.

[8]  Chunlei Liu,et al.  Whole brain susceptibility mapping using compressed sensing , 2012, Magnetic resonance in medicine.

[9]  S. Kwon,et al.  Cilostazol Prevents the Progression of the Symptomatic Intracranial Arterial Stenosis: The Multicenter Double-Blind Placebo-Controlled Trial of Cilostazol in Symptomatic Intracranial Arterial Stenosis , 2005, Stroke.

[10]  A A Lammertsma,et al.  Correction for the Presence of Intravascular Oxygen-15 in the Steady-State Technique for Measuring Regional Oxygen Extraction Ratio in the Brain: 1. Description of the Method , 1983, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[11]  Tian Liu,et al.  Oxygen extraction fraction measurement using quantitative susceptibility mapping: Comparison with positron emission tomography , 2016, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[12]  Ferdinand Schweser,et al.  Quantitative susceptibility mapping for investigating subtle susceptibility variations in the human brain , 2012, NeuroImage.

[13]  John Ashburner,et al.  SPM: A history , 2012, NeuroImage.

[14]  J. Hendrikse,et al.  Calibrated MRI to Evaluate Cerebral Hemodynamics in Patients with an Internal Carotid Artery Occlusion , 2015, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[15]  Risto A. Kauppinen,et al.  Quantitative assessment of blood flow, blood volume and blood oxygenation effects in functional magnetic resonance imaging , 1998, Nature Medicine.

[16]  Kohsuke Kudo,et al.  Susceptibility‐Weighted Phase Imaging and Oxygen Extraction Fraction Measurement during Sedation and Sedation Recovery using 7T MRI , 2015, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

[17]  J. Duyn,et al.  Magnetic susceptibility mapping of brain tissue in vivo using MRI phase data , 2009, Magnetic resonance in medicine.

[18]  Elfar Adalsteinsson,et al.  Phase‐based regional oxygen metabolism (PROM) using MRI , 2012, Magnetic resonance in medicine.

[19]  Pascal Spincemaille,et al.  Quantitative mapping of cerebral metabolic rate of oxygen (CMRO2) using quantitative susceptibility mapping (QSM) , 2015, Magnetic resonance in medicine.

[20]  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.

[21]  Z. Liu,et al.  Cortical Cerebral Blood Flow, Oxygen Extraction Fraction, and Metabolic Rate in Patients with Middle Cerebral Artery Stenosis or Acute Stroke , 2016, American Journal of Neuroradiology.

[22]  Hiroki Shirato,et al.  Mapping of cerebral oxygen extraction fraction changes with susceptibility-weighted phase imaging. , 2011, Radiology.

[23]  Shunrou Fujiwara,et al.  Central Benzodiazepine Receptor Binding Potential and CBF Images on SPECT Correlate with Oxygen Extraction Fraction Images on PET in the Cerebral Cortex with Unilateral Major Cerebral Artery Occlusive Disease , 2011, The Journal of Nuclear Medicine.

[24]  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.

[25]  Yo Taniguchi,et al.  Quantitative Susceptibility Mapping Using the Multiple Dipole-inversion Combination with k-space Segmentation Method , 2017, Magnetic resonance in medical sciences : MRMS : an official journal of Japan Society of Magnetic Resonance in Medicine.

[26]  Richard G. Wise,et al.  Measurement of OEF and absolute CMRO2: MRI-based methods using interleaved and combined hypercapnia and hyperoxia , 2013, NeuroImage.

[27]  Zhaoxia Wang,et al.  Quantitative Measurement of Cerebral Oxygen Extraction Fraction Using MRI in Patients with MELAS , 2013, PloS one.

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

[29]  Yi Wang,et al.  Morphology enabled dipole inversion (MEDI) from a single‐angle acquisition: Comparison with COSMOS in human brain imaging , 2011, Magnetic resonance in medicine.

[30]  L. Wilkins.  North American Symptomatic Carotid Endarterectomy Trial. Methods, patient characteristics, and progress. , 1991, Stroke.

[31]  H. Fukuyama,et al.  Is misery perfusion still a predictor of stroke in symptomatic major cerebral artery disease? , 2012, Brain : a journal of neurology.

[32]  G. Zaharchuk,et al.  Imaging Brain Oxygenation with MRI Using Blood Oxygenation Approaches: Methods, Validation, and Clinical Applications , 2013, American Journal of Neuroradiology.

[33]  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.

[34]  Henry Rusinek,et al.  Characterizing Brain Oxygen Metabolism in Patients with Multiple Sclerosis with T2-Relaxation-Under-Spin-Tagging MRI , 2012, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[35]  A. Wilman,et al.  Background field removal using spherical mean value filtering and Tikhonov regularization , 2014, Magnetic resonance in medicine.

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

[37]  S. Kwon,et al.  Cilostazol Prevents the Progression of the Symptomatic Intracranial Arterial Stenosis: The Multicenter Double-Blind Placebo-Controlled Trial of Cilostazol in Symptomatic Intracranial Arterial Stenosis , 2005 .

[38]  Guido Gerig,et al.  User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability , 2006, NeuroImage.

[39]  P. Jezzard,et al.  Quantitative measurement of cerebral physiology using respiratory-calibrated MRI , 2012, NeuroImage.