Reproducibility of multiphase pseudo-continuous arterial spin labeling and the effect of post-processing analysis methods

Arterial spin labeling (ASL) is an emerging MRI technique for non-invasive measurement of cerebral blood flow (CBF). Compared to invasive perfusion imaging modalities, ASL suffers from low sensitivity due to poor signal-to-noise ratio (SNR), susceptibility to motion artifacts and low spatial resolution, all of which limit its reliability. In this work, the effects of various state of the art image processing techniques for addressing these ASL limitations are investigated. A processing pipeline consisting of motion correction, ASL motion correction imprecision removal, temporal and spatial filtering, partial volume effect correction, and CBF quantification was developed and assessed. To further improve the SNR for pseudo-continuous ASL (PCASL) by accounting for errors in tagging efficiency, the data from multiphase (MP) acquisitions were analyzed using a novel weighted-averaging scheme. The performances of each step in terms of SNR and reproducibility were evaluated using test-retest ASL data acquired from 12 young healthy subjects. The proposed processing pipeline was shown to improve the within-subject coefficient of variation and regional reproducibility by 17% and 16%, respectively, compared to CBF maps computed following motion correction but without the other processing steps. The CBF measurements of MP-PCASL compared to PCASL had on average 23% and 10% higher SNR and reproducibility, respectively.

[1]  R. Buxton,et al.  Quantitative imaging of perfusion using a single subtraction (QUIPSS and QUIPSS II) , 1998 .

[2]  Xiaoyun Liang,et al.  A variable flip angle-based method for reducing blurring in 3D GRASE ASL , 2014, Physics in medicine and biology.

[3]  Daniel Y. Kimberg,et al.  Empirical analyses of null-hypothesis perfusion FMRI data at 1.5 and 4 T , 2003, NeuroImage.

[4]  Hesamoddin Jahanian,et al.  Quantitative analysis of arterial spin labeling FMRI data using a general linear model. , 2010, Magnetic resonance imaging.

[5]  Alessandra Bertoldo,et al.  Investigation of brain hemodynamic changes induced by active and passive movements: A combined arterial spin labeling–BOLD fMRI study , 2014, Journal of magnetic resonance imaging : JMRI.

[6]  N. Tzourio-Mazoyer,et al.  Automated Anatomical Labeling of Activations in SPM Using a Macroscopic Anatomical Parcellation of the MNI MRI Single-Subject Brain , 2002, NeuroImage.

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

[8]  X Golay,et al.  Non-invasive Measurement of Perfusion: a Critical Review of Arterial Spin Labelling Techniques , 2022 .

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

[10]  Peter C M van Zijl,et al.  An account of the discrepancy between MRI and PET cerebral blood flow measures. A high‐field MRI investigation , 2006, NMR in biomedicine.

[11]  Alan Connelly,et al.  Reduction of errors in ASL cerebral perfusion and arterial transit time maps using image de‐noising , 2010, Magnetic resonance in medicine.

[12]  Gaohong Wu,et al.  Reliability and precision of pseudo‐continuous arterial spin labeling perfusion MRI on 3.0 T and comparison with 15O‐water PET in elderly subjects at risk for Alzheimer's disease , 2010, NMR in biomedicine.

[13]  Joseph A Maldjian,et al.  Clinical applications of arterial spin labeling , 2013, NMR in biomedicine.

[14]  Matthias Günther,et al.  Comparison of Arterial Spin-Labeling Techniques and Dynamic Susceptibility-Weighted Contrast-Enhanced MRI in Perfusion Imaging of Normal Brain Tissue , 2003, Investigative radiology.

[15]  W. Strik,et al.  Comparison of spatial and temporal pattern for fMRI obtained with BOLD and arterial spin labeling , 2006, Journal of Neural Transmission.

[16]  Thomas T. Liu,et al.  A component based noise correction method (CompCor) for BOLD and perfusion based fMRI , 2007, NeuroImage.

[17]  Xin Lou,et al.  Reliability of Three-Dimensional Pseudo-Continuous Arterial Spin Labeling MR Imaging for Measuring Visual Cortex Perfusion on Two 3T Scanners , 2013, PloS one.

[18]  S Warach,et al.  A general kinetic model for quantitative perfusion imaging with arterial spin labeling , 1998, Magnetic resonance in medicine.

[19]  M. Bronskill,et al.  T1, T2 relaxation and magnetization transfer in tissue at 3T , 2005, Magnetic resonance in medicine.

[20]  Ivan Pedrosa,et al.  Strategies for reducing respiratory motion artifacts in renal perfusion imaging with arterial spin labeling , 2009, Magnetic resonance in medicine.

[21]  Xavier Golay,et al.  Improved partial volume correction of ASL images using 3D kernels , 2012 .

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

[23]  Xiaoyun Liang,et al.  A k‐space sharing 3D GRASE pseudocontinuous ASL method for whole‐brain resting‐state functional connectivity , 2012, Int. J. Imaging Syst. Technol..

[24]  R. Kraft,et al.  3D GRASE PROPELLER: Improved image acquisition technique for arterial spin labeling perfusion imaging , 2011, Magnetic resonance in medicine.

[25]  Koenraad Van Leemput,et al.  Automated model-based tissue classification of MR images of the brain , 1999, IEEE Transactions on Medical Imaging.

[26]  Christian Barillot,et al.  Robust Cerebral Blood Flow Map Estimation in Arterial Spin Labeling , 2012, MBIA.

[27]  Josef Pfeuffer,et al.  Comparison of pulsed arterial spin labeling encoding schemes and absolute perfusion quantification. , 2009, Magnetic resonance imaging.

[28]  R E Lenkinski,et al.  Magnetic resonance imaging of the brain: Blood partition coefficient for water: Application to spin‐tagging measurement of perfusion , 1996, Journal of magnetic resonance imaging : JMRI.

[29]  Weiying Dai,et al.  Sensitivity calibration with a uniform magnetization image to improve arterial spin labeling perfusion quantification , 2011, Magnetic resonance in medicine.

[30]  Olaf B. Paulson,et al.  Arterial spin labeling in the presence of severe motion , 2005 .

[31]  Thomas T. Liu,et al.  A signal processing model for arterial spin labeling functional MRI , 2005, NeuroImage.

[32]  Marion Smits,et al.  Title 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 , 2014 .

[33]  David L. Thomas,et al.  Measuring Cerebral Blood Flow Using Magnetic Resonance Imaging Techniques , 1999, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[34]  Donald S. Williams,et al.  Perfusion imaging , 1992, Magnetic resonance in medicine.

[35]  Ze Wang,et al.  Improving cerebral blood flow quantification for arterial spin labeled perfusion MRI by removing residual motion artifacts and global signal fluctuations. , 2012, Magnetic resonance imaging.

[36]  A. Connelly,et al.  Improved partial volume correction for single inversion time arterial spin labeling data , 2013, Magnetic resonance in medicine.

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

[38]  J. Detre,et al.  A theoretical and experimental investigation of the tagging efficiency of pseudocontinuous arterial spin labeling , 2007, Magnetic resonance in medicine.

[39]  Xiaoyun Liang,et al.  Voxel-Wise Functional Connectomics Using Arterial Spin Labeling Functional Magnetic Resonance Imaging: The Role of Denoising , 2015, Brain Connect..

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

[41]  Bing Wu,et al.  Intra‐ and interscanner reliability and reproducibility of 3D whole‐brain pseudo‐continuous arterial spin‐labeling MR perfusion at 3T , 2014, Journal of magnetic resonance imaging : JMRI.

[42]  Peter C M van Zijl,et al.  Theoretical and experimental investigation of the VASO contrast mechanism , 2006, Magnetic resonance in medicine.

[43]  Hanzhang Lu,et al.  Detrimental effects of BOLD signal in arterial spin labeling fMRI at high field strength , 2006, Magnetic resonance in medicine.

[44]  Wen-Ming Luh,et al.  Pseudo‐continuous arterial spin labeling at 7 T for human brain: Estimation and correction for off‐resonance effects using a Prescan , 2013, Magnetic resonance in medicine.

[45]  J. Detre,et al.  Continuous arterial spin labeling perfusion measurements using single shot 3D GRASE at 3 T , 2005, Magnetic resonance in medicine.

[46]  J. Duyn,et al.  High‐sensitivity single‐shot perfusion‐weighted fMRI † , 2001, Magnetic resonance in medicine.

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

[48]  Ze Wang,et al.  Empirical optimization of ASL data analysis using an ASL data processing toolbox: ASLtbx. , 2008, Magnetic resonance imaging.

[49]  Xavier Golay,et al.  Determining the longitudinal relaxation time (T1) of blood at 3.0 Tesla , 2004, Magnetic resonance in medicine.

[50]  R. Kraft,et al.  A fast, effective filtering method for improving clinical pulsed arterial spin labeling MRI , 2009, Journal of magnetic resonance imaging : JMRI.

[51]  J. Detre,et al.  To smooth or not to smooth? ROC analysis of perfusion fMRI data. , 2005, Magnetic resonance imaging.

[52]  Xiaoyun Liang,et al.  Graph analysis of resting-state ASL perfusion MRI data: Nonlinear correlations among CBF and network metrics , 2014, NeuroImage.

[53]  Emily Kilroy,et al.  Reliability of two‐dimensional and three‐dimensional pseudo‐continuous arterial spin labeling perfusion MRI in elderly populations: Comparison with 15o‐water positron emission tomography , 2014, Journal of magnetic resonance imaging : JMRI.

[54]  Youngkyoo Jung,et al.  Multiphase pseudocontinuous arterial spin labeling (MP‐PCASL) for robust quantification of cerebral blood flow , 2010, Magnetic resonance in medicine.

[55]  I. Tracey,et al.  Optimization and Reliability of Multiple Postlabeling Delay Pseudo-Continuous Arterial Spin Labeling during Rest and Stimulus-Induced Functional Task Activation , 2014, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.