Regional Reproducibility of BOLD Calibration Parameter M, OEF and Resting-State CMRO2 Measurements with QUO2 MRI

The current generation of calibrated MRI methods goes beyond simple localization of task-related responses to allow the mapping of resting-state cerebral metabolic rate of oxygen (CMRO2) in micromolar units and estimation of oxygen extraction fraction (OEF). Prior to the adoption of such techniques in neuroscience research applications, knowledge about the precision and accuracy of absolute estimates of CMRO2 and OEF is crucial and remains unexplored to this day. In this study, we addressed the question of methodological precision by assessing the regional inter-subject variance and intra-subject reproducibility of the BOLD calibration parameter M, OEF, O2 delivery and absolute CMRO2 estimates derived from a state-of-the-art calibrated BOLD technique, the QUantitative O2 (QUO2) approach. We acquired simultaneous measurements of CBF and R2* at rest and during periods of hypercapnia (HC) and hyperoxia (HO) on two separate scan sessions within 24 hours using a clinical 3 T MRI scanner. Maps of M, OEF, oxygen delivery and CMRO2, were estimated from the measured end-tidal O2, CBF0, CBFHC/HO and R2*HC/HO. Variability was assessed by computing the between-subject coefficients of variation (bwCV) and within-subject CV (wsCV) in seven ROIs. All tests GM-averaged values of CBF0, M, OEF, O2 delivery and CMRO2 were: 49.5 ± 6.4 mL/100 g/min, 4.69 ± 0.91%, 0.37 ± 0.06, 377 ± 51 μmol/100 g/min and 143 ± 34 μmol/100 g/min respectively. The variability of parameter estimates was found to be the lowest when averaged throughout all GM, with general trends toward higher CVs when averaged over smaller regions. Among the MRI measurements, the most reproducible across scans was R2*0 (wsCVGM = 0.33%) along with CBF0 (wsCVGM = 3.88%) and R2*HC (wsCVGM = 6.7%). CBFHC and R2*HO were found to have a higher intra-subject variability (wsCVGM = 22.4% and wsCVGM = 16% respectively), which is likely due to propagation of random measurement errors, especially for CBFHC due to the low contrast-to-noise ratio intrinsic to ASL. Reproducibility of the QUO2 derived estimates were computed, yielding a GM intra-subject reproducibility of 3.87% for O2 delivery, 16.8% for the M value, 13.6% for OEF and 15.2% for CMRO2. Although these results focus on the precision of the QUO2 method, rather than the accuracy, the information will be useful for calculation of statistical power in future validation studies and ultimately for research applications of the method. The higher test-retest variability for the more extensively modeled parameters (M, OEF, and CMRO2) highlights the need for further improvement of acquisition methods to reduce noise levels.

[1]  Arno Klein,et al.  101 Labeled Brain Images and a Consistent Human Cortical Labeling Protocol , 2012, Front. Neurosci..

[2]  P. Tofts,et al.  Normal cerebral perfusion measurements using arterial spin labeling: Reproducibility, stability, and age and gender effects , 2004, Magnetic resonance in medicine.

[3]  Claudine Joëlle Gauthier,et al.  Absolute quantification of resting oxygen metabolism and metabolic reactivity during functional activation using QUO2 MRI , 2012, NeuroImage.

[4]  D. Altman,et al.  STATISTICAL METHODS FOR ASSESSING AGREEMENT BETWEEN TWO METHODS OF CLINICAL MEASUREMENT , 1986, The Lancet.

[5]  J. Detre,et al.  Assessment of cerebral blood flow in Alzheimer's disease by spin‐labeled magnetic resonance imaging , 2000, Annals of neurology.

[6]  D. Feinberg,et al.  Single‐shot 3D imaging techniques improve arterial spin labeling perfusion measurements , 2005, Magnetic resonance in medicine.

[7]  Kawin Setsompop,et al.  Ultra-fast MRI of the human brain with simultaneous multi-slice imaging. , 2013, Journal of magnetic resonance.

[8]  A. McLaughlin,et al.  Role of Nitric Oxide in Regulating Cerebrocortical Oxygen Consumption and Blood Flow during Hypercapnia , 1994, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[9]  Jeroen Hendrikse,et al.  In vivo quantification of hyperoxic arterial blood water T1 , 2015, NMR in biomedicine.

[10]  E. Cadenas,et al.  Shift in brain metabolism in late onset Alzheimer's disease: implications for biomarkers and therapeutic interventions. , 2011, Molecular aspects of medicine.

[11]  Hanzhang Lu,et al.  Noninvasive quantification of whole‐brain cerebral metabolic rate of oxygen (CMRO2) by MRI , 2009, Magnetic resonance in medicine.

[12]  R. Frackowiak,et al.  Quantitative Measurement of Regional Cerebral Blood Flow and Oxygen Metabolism in Man Using 15O and Positron Emission Tomography: Theory, Procedure, and Normal Values , 1980, Journal of computer assisted tomography.

[13]  B. Avants,et al.  Longitudinal reproducibility and accuracy of pseudo-continuous arterial spin-labeled perfusion MR imaging in typically developing children. , 2012, Radiology.

[14]  John A. Detre,et al.  Physiological Modulations in Arterial Spin Labeling Perfusion Magnetic Resonance Imaging , 2009, IEEE Transactions on Medical Imaging.

[15]  A. Padhani,et al.  Reproducibility of quantitative dynamic MRI of normal human tissues , 2002, NMR in biomedicine.

[16]  D J Brooks,et al.  Dexamethasone treatment of brain tumor patients , 1985, Neurology.

[17]  Peter Jezzard,et al.  Cerebral Perfusion Response to Hyperoxia , 2007, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[18]  Feng Xu,et al.  The Influence of Carbon Dioxide on Brain Activity and Metabolism in Conscious Humans , 2011, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[19]  N. Schuff,et al.  Pattern of cerebral hypoperfusion in Alzheimer disease and mild cognitive impairment measured with arterial spin-labeling MR imaging: initial experience. , 2005, Radiology.

[20]  D. Louis Collins,et al.  Automatic 3‐D model‐based neuroanatomical segmentation , 1995 .

[21]  R. Hoge,et al.  Comparison of Cerebral Vascular Reactivity Measures Obtained Using Breath-Holding and CO2 Inhalation , 2013, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[22]  Richard G. Wise,et al.  Measurement of oxygen extraction fraction (OEF): An optimized BOLD signal model for use with hypercapnic and hyperoxic calibration , 2016, NeuroImage.

[23]  John D Pickard,et al.  Intersubject Variability and Reproducibility of 15O PET Studies , 2006, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[24]  N. Logothetis,et al.  Direct measurement of oxygen extraction with fMRI using 6% CO2 inhalation. , 2008, Magnetic resonance imaging.

[25]  G. Zaharchuk,et al.  Recommended implementation of arterial spin-labeled perfusion MRI for clinical applications: A consensus of the ISMRM perfusion study group and the European consortium for ASL in dementia. , 2015, Magnetic resonance in medicine.

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

[27]  Peter Jezzard,et al.  Comparison of hypercapnia‐based calibration techniques for measurement of cerebral oxygen metabolism with MRI , 2009, Magnetic resonance in medicine.

[28]  Peter T Fox,et al.  Evaluation of MRI models in the measurement of CMRO2 and its relationship with CBF , 2008, Magnetic resonance in medicine.

[29]  Richard S. J. Frackowiak,et al.  Cerebral blood flow, blood volume and oxygen utilization. Normal values and effect of age. , 1990, Brain : a journal of neurology.

[30]  Gary F. Egan,et al.  Regional reproducibility of calibrated BOLD functional MRI: Implications for the study of cognition and plasticity , 2014, NeuroImage.

[31]  Richard B. Buxton,et al.  Regional differences in the coupling of cerebral blood flow and oxygen metabolism changes in response to activation: Implications for BOLD-fMRI , 2008, NeuroImage.

[32]  Irene Tracey,et al.  Quantitative assessment of the reproducibility of functional activation measured with BOLD and MR perfusion imaging: Implications for clinical trial design , 2005, NeuroImage.

[33]  Jeroen Hendrikse,et al.  Bolus Arrival Time and Cerebral Blood Flow Responses to Hypercarbia , 2014, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[34]  M Liotti,et al.  Neuroimaging of cerebral activations and deactivations associated with hypercapnia and hunger for air. , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[35]  M. Poulin,et al.  Dynamics of the cerebral blood flow response to step changes in end-tidal PCO2 and PO2 in humans. , 1996, Journal of applied physiology.

[36]  B R Rosen,et al.  Mr contrast due to intravascular magnetic susceptibility perturbations , 1995, Magnetic resonance in medicine.

[37]  Joseph A Maldjian,et al.  Arterial transit time imaging with flow encoding arterial spin tagging (FEAST) , 2003, Magnetic resonance in medicine.

[38]  Peter Jezzard,et al.  Assessment of arterial arrival times derived from multiple inversion time pulsed arterial spin labeling MRI , 2010, Magnetic resonance in medicine.

[39]  Isabelle Lajoie,et al.  Test–retest reliability of cerebral blood flow and blood oxygenation level‐dependent responses to hypercapnia and hyperoxia using dual‐echo pseudo‐continuous arterial spin labeling and step changes in the fractional composition of inspired gases , 2015, Journal of magnetic resonance imaging : JMRI.

[40]  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.

[41]  Hesamoddin Jahanian,et al.  B0 field inhomogeneity considerations in pseudo‐continuous arterial spin labeling (pCASL): effects on tagging efficiency and correction strategy , 2011, NMR in biomedicine.

[42]  Daniel Gallichan,et al.  Variation in the shape of pulsed arterial spin labeling kinetic curves across the healthy human brain and its implications for CBF quantification , 2009, Magnetic resonance in medicine.

[43]  John A Detre,et al.  Precision of the CASL‐perfusion MRI technique for the measurement of cerebral blood flow in whole brain and vascular territories , 2003, Journal of magnetic resonance imaging : JMRI.

[44]  Claudine Joëlle Gauthier,et al.  Elimination of visually evoked BOLD responses during carbogen inhalation: Implications for calibrated MRI , 2011, NeuroImage.

[45]  J D Pickard,et al.  Influence of baseline hematocrit on between-subject BOLD signal change using gradient echo and asymmetric spin echo EPI. , 2003, Magnetic resonance imaging.

[46]  Richard B. Buxton,et al.  Reproducibility of BOLD, perfusion, and CMRO2 measurements with calibrated-BOLD fMRI , 2007, NeuroImage.

[47]  R W McPherson,et al.  Changes in Cerebral CO2 Responsivity over Time During Isoflurane Anesthesia in the Dog , 1991, Journal of neurosurgical anesthesiology.

[48]  Ronald Boellaard,et al.  Day-to-Day Test–Retest Variability of CBF, CMRO2, and OEF Measurements Using Dynamic 15O PET Studies , 2010, Molecular Imaging and Biology.

[49]  N. Schuff,et al.  Hypoperfusion in frontotemporal dementia and Alzheimer disease by arterial spin labeling MRI , 2006, Neurology.

[50]  Shintaro Funahashi,et al.  Saccade-related activity in the prefrontal cortex: its role in eye movement control and cognitive functions , 2014, Front. Integr. Neurosci..

[51]  D G Altman,et al.  Statistics Notes: Measurement error proportional to the mean , 1996, BMJ.

[52]  G. Zaharchuk,et al.  Noninvasive Imaging of Quantitative Cerebral Blood Flow Changes during 100% Oxygen Inhalation Using Arterial Spin-Labeling MR Imaging , 2008, American Journal of Neuroradiology.

[53]  T. Brown,et al.  Regression algorithm correcting for partial volume effects in arterial spin labeling MRI , 2008, Magnetic resonance in medicine.

[54]  G. Bruce Pike,et al.  Improved fMRI calibration: Precisely controlled hyperoxic versus hypercapnic stimuli , 2011, NeuroImage.

[55]  J. Severinghaus,et al.  Water vapor calibration errors in some capnometers: respiratory conventions misunderstood by manufacturers? , 1989, Anesthesiology.

[56]  D. Weinberger,et al.  Noise reduction in 3D perfusion imaging by attenuating the static signal in arterial spin tagging (ASSIST) , 2000, Magnetic resonance in medicine.

[57]  B L Short,et al.  Cerebral blood flow and metabolism during and after prolonged hypercapnia in newborn lambs , 2000, Critical care medicine.

[58]  Iwao Kanno,et al.  Database of normal human cerebral blood flow, cerebral blood volume, cerebral oxygen extraction fraction and cerebral metabolic rate of oxygen measured by positron emission tomography with 15O-labelled carbon dioxide or water, carbon monoxide and oxygen: a multicentre study in Japan , 2004, European Journal of Nuclear Medicine and Molecular Imaging.

[59]  D. Alsop,et al.  Efficiency of inversion pulses for background suppressed arterial spin labeling , 2005, Magnetic resonance in medicine.

[60]  Todd B. Parrish,et al.  Caffeine's effects on cerebrovascular reactivity and coupling between cerebral blood flow and oxygen metabolism , 2009, NeuroImage.

[61]  Thomas T. Liu,et al.  Caffeine-induced uncoupling of cerebral blood flow and oxygen metabolism: A calibrated BOLD fMRI study , 2008, NeuroImage.

[62]  Stephen M. Smith,et al.  A global optimisation method for robust affine registration of brain images , 2001, Medical Image Anal..

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

[64]  Felix W Wehrli,et al.  MRI Estimation of Global Brain Oxygen Consumption Rate , 2010, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[65]  J. J. Chen,et al.  BOLD‐specific cerebral blood volume and blood flow changes during neuronal activation in humans , 2009, NMR in biomedicine.

[66]  Feng Xu,et al.  Estimation of labeling efficiency in pseudocontinuous arterial spin labeling , 2010, Magnetic resonance in medicine.

[67]  G H Glover,et al.  Image‐based method for retrospective correction of physiological motion effects in fMRI: RETROICOR , 2000, Magnetic resonance in medicine.

[68]  Claudine Joëlle Gauthier,et al.  Magnetic resonance imaging of resting OEF and CMRO2 using a generalized calibration model for hypercapnia and hyperoxia , 2012, NeuroImage.

[69]  Yuki Shinohara,et al.  Interindividual Variations of Cerebral Blood Flow, Oxygen Delivery, and Metabolism in Relation to Hemoglobin Concentration Measured by Positron Emission Tomography in Humans , 2010, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[70]  Ravinder Reddy,et al.  Absolute cerebral blood flow quantification with pulsed arterial spin labeling during hyperoxia corrected with the simultaneous measurement of the longitudinal relaxation time of arterial blood , 2012, Magnetic resonance in medicine.

[71]  Michael A. Chappell,et al.  Effects of background suppression on the sensitivity of dual-echo arterial spin labeling MRI for BOLD and CBF signal changes , 2014, NeuroImage.

[72]  Peiying Liu,et al.  Effect of Hypoxia and Hyperoxia on Cerebral Blood Flow, Blood Oxygenation, and Oxidative Metabolism , 2012, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[73]  Yufen Chen,et al.  Test–retest reliability of arterial spin labeling with common labeling strategies , 2011, Journal of magnetic resonance imaging : JMRI.

[74]  A. Fleisher,et al.  Effects of aging on cerebral blood flow, oxygen metabolism, and blood oxygenation level dependent responses to visual stimulation , 2009, Human brain mapping.

[75]  D. Alsop,et al.  Continuous flow‐driven inversion for arterial spin labeling using pulsed radio frequency and gradient fields , 2008, Magnetic resonance in medicine.

[76]  Yaakov Stern,et al.  Multivariate and Univariate Analysis of Continuous Arterial Spin Labeling Perfusion MRI in Alzheimer's Disease , 2008, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[77]  J. Detre,et al.  Magnetic resonance perfusion imaging in acute ischemic stroke using continuous arterial spin labeling. , 2000, Stroke.

[78]  Donald S. Williams,et al.  NMR Measurement of Perfusion Using Arterial Spin Labeling Without Saturation of Macromolecular Spins , 1995, Magnetic resonance in medicine.

[79]  E. Kato,et al.  Cerebral blood flow and oxygen metabolism in senile dementia of Alzheimer's type and vascular dementia with deep white matter changes , 1998, Neuroradiology.

[80]  Tristan Glatard,et al.  CBRAIN: a web-based, distributed computing platform for collaborative neuroimaging research , 2014, Front. Neuroinform..

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

[82]  Chen Lin,et al.  Regional reproducibility of pulsed arterial spin labeling perfusion imaging at 3T , 2011, NeuroImage.

[83]  M Liotti,et al.  Brain responses associated with consciousness of breathlessness (air hunger). , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[84]  G. Bruce Pike,et al.  MRI measurement of the BOLD-specific flow–volume relationship during hypercapnia and hypocapnia in humans , 2010, NeuroImage.

[85]  S. Francis,et al.  An improved method for acquiring cerebrovascular reactivity maps , 2011, Magnetic resonance in medicine.

[86]  Isabelle Lajoie,et al.  A simple breathing circuit allowing precise control of inspiratory gases for experimental respiratory manipulations , 2014, BMC Research Notes.

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

[88]  Richard Wise,et al.  A calibration method for quantitative BOLD fMRI based on hyperoxia , 2007, NeuroImage.

[89]  R. Hoge,et al.  A generalized procedure for calibrated MRI incorporating hyperoxia and hypercapnia , 2013, Human brain mapping.