Applications of arterial spin labeled MRI in the brain

Perfusion provides oxygen and nutrients to tissues and is closely tied to tissue function while disorders of perfusion are major sources of medical morbidity and mortality. It has been almost two decades since the use of arterial spin labeling (ASL) for noninvasive perfusion imaging was first reported. While initial ASL magnetic resonance imaging (MRI) studies focused primarily on technological development and validation, a number of robust ASL implementations have emerged, and ASL MRI is now also available commercially on several platforms. As a result, basic science and clinical applications of ASL MRI have begun to proliferate. Although ASL MRI can be carried out in any organ, most studies to date have focused on the brain. This review covers selected research and clinical applications of ASL MRI in the brain to illustrate its potential in both neuroscience research and clinical care. J. Magn. Reson. Imaging 2012;35:1026‐1037. © 2012 Wiley Periodicals, Inc.

[1]  T. Floyd,et al.  Skeletal muscle microvascular flow in progressive peripheral artery disease: assessment with continuous arterial spin-labeling perfusion magnetic resonance imaging. , 2009, Journal of the American College of Cardiology.

[2]  A. Horn,et al.  Baseline brain perfusion and working memory capacity: a neuroimaging study , 2008, Neuroreport.

[3]  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.

[4]  R. Kraft,et al.  Arterial Spin-Labeled Magnetic Resonance Imaging in Hyperperfused Seizure Focus: A Case Report , 2008, Journal of computer assisted tomography.

[5]  Wen-Chau Wu,et al.  Velocity‐selective arterial spin labeling , 2006, Magnetic resonance in medicine.

[6]  J. Detre,et al.  Neuroimaging in Developmental Clinical Neuroscience: Arterial spin labeling perfusion magnetic resonance imaging in developmental neuroscience , 2009 .

[7]  Shana A. Hall,et al.  Alcohol effects on cerebral blood flow in subjects with low and high responses to alcohol. , 2011, Alcoholism, clinical and experimental research.

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

[9]  Seong-Gi Kim,et al.  Functional MRI of calcium‐dependent synaptic activity: Cross correlation with CBF and BOLD measurements , 2000, Magnetic resonance in medicine.

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

[11]  John Pluta,et al.  Gender difference in neural response to psychological stress. , 2007, Social cognitive and affective neuroscience.

[12]  J. Detre,et al.  Perfusion functional MRI reveals cerebral blood flow pattern under psychological stress. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[13]  R. Gonzalez,et al.  Glioma recurrence versus radiation necrosis? A pilot comparison of arterial spin-labeled, dynamic susceptibility contrast enhanced MRI, and FDG-PET imaging. , 2010, Academic radiology.

[14]  Weiying Dai,et al.  Time-resolved vessel-selective digital subtraction MR angiography of the cerebral vasculature with arterial spin labeling. , 2010, Radiology.

[15]  Karl J. Friston,et al.  Voxel-Based Morphometry—The Methods , 2000, NeuroImage.

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

[17]  J. Detre,et al.  Arteriovenous Shunt Visualization in Arteriovenous Malformations with Arterial Spin-Labeling MR Imaging , 2008, American Journal of Neuroradiology.

[18]  J. Detre,et al.  Neuropsychological and perfusion MR imaging correlates of revascularization in a case of moyamoya syndrome. , 2006, AJNR. American journal of neuroradiology.

[19]  Eliza Congdon,et al.  Neural correlates of epigenesis , 2006, Proceedings of the National Academy of Sciences.

[20]  Jesse J. Suh,et al.  Effects of varenicline on smoking cue–triggered neural and craving responses. , 2011, Archives of general psychiatry.

[21]  R E Lenkinski,et al.  Renal perfusion in humans: MR imaging with spin tagging of arterial water. , 1995, Radiology.

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

[23]  M. D’Esposito,et al.  Empirical analyses of BOLD fMRI statistics. I. Spatially unsmoothed data collected under null-hypothesis conditions. , 1997, NeuroImage.

[24]  J. Detre,et al.  Measurement of cerebral blood flow in rat brain by 19F‐NMR detection of trifluoromethane washout , 1990, Magnetic resonance in medicine.

[25]  J. Detre,et al.  Quantification of Cerebral Blood Flow as Biomarker of Drug Effect: Arterial Spin Labeling phMRI After a Single Dose of Oral Citalopram , 2011, Clinical pharmacology and therapeutics.

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

[27]  Peter Jezzard,et al.  Selective arterial spin labeling (SASL): Perfusion territory mapping of selected feeding arteries tagged using two‐dimensional radiofrequency pulses , 2003, Magnetic resonance in medicine.

[28]  J. Ackerman,et al.  Deuterium nuclear magnetic resonance measurements of blood flow and tissue perfusion employing 2H2O as a freely diffusible tracer. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[29]  M. Phelps,et al.  Maturational changes in cerebral function in infants determined by 18FDG positron emission tomography. , 1986, Science.

[30]  Lukas Scheef,et al.  Resting-state perfusion in nonmedicated schizophrenic patients: a continuous arterial spin-labeling 3.0-T MR study. , 2010, Radiology.

[31]  J. Detre,et al.  Perfusion magnetic resonance imaging with continuous arterial spin labeling: methods and clinical applications in the central nervous system. , 1999, European journal of radiology.

[32]  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.

[33]  Danny J. J. Wang,et al.  Cerebral blood flow changes associated with different meditation practices and perceived depth of meditation , 2011, Psychiatry Research: Neuroimaging.

[34]  J. Detre,et al.  Nicotine abstinence-induced cerebral blood flow changes by genotype , 2008, Neuroscience Letters.

[35]  Marcus E Raichle,et al.  Neuroscience. The brain's dark energy. , 2006, Science.

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

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

[38]  J. Detre,et al.  Arterial spin labeling blood flow MRI: its role in the early characterization of Alzheimer's disease. , 2010, Journal of Alzheimer's disease : JAD.

[39]  Maite Aznárez-Sanado,et al.  Effects on resting cerebral blood flow and functional connectivity induced by metoclopramide: a perfusion MRI study in healthy volunteers , 2011, British journal of pharmacology.

[40]  John A. Detre,et al.  Imaging brain fatigue from sustained mental workload: An ASL perfusion study of the time-on-task effect , 2010, NeuroImage.

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

[42]  David G Norris,et al.  Continuous artery‐selective spin labeling (CASSL) , 2005, Magnetic resonance in medicine.

[43]  J. Detre,et al.  Arterial spin labeling perfusion fMRI with very low task frequency , 2003, Magnetic resonance in medicine.

[44]  R. Ehrman,et al.  Limbic Activation to Cigarette Smoking Cues Independent of Nicotine Withdrawal: A Perfusion fMRI Study , 2007, Neuropsychopharmacology.

[45]  David C. Alsop,et al.  Increased cerebral perfusion in adult attention deficit hyperactivity disorder is normalised by stimulant treatment: A non-invasive MRI pilot study , 2008, NeuroImage.

[46]  John A. Detre,et al.  Genetic Variation in Serotonin Transporter Alters Resting Brain Function in Healthy Individuals , 2007, Biological Psychiatry.

[47]  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.

[48]  Thomas T. Liu,et al.  Caffeine alters the temporal dynamics of the visual BOLD response , 2004, NeuroImage.

[49]  Stefan Golaszewski,et al.  Does caffeine modulate verbal working memory processes? An fMRI study , 2008, NeuroImage.

[50]  William D. Gaillard,et al.  Usefulness of pulsed arterial spin labeling MR imaging in mesial temporal lobe epilepsy , 2008, Epilepsy Research.

[51]  Hengyi Rao,et al.  Imaging brain activity during natural vision using CASL perfusion fMRI , 2007, Human brain mapping.

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

[53]  William Vennart,et al.  Beyond Patient Reported Pain: Perfusion Magnetic Resonance Imaging Demonstrates Reproducible Cerebral Representation of Ongoing Post-Surgical Pain , 2011, PloS one.

[54]  J. Detre,et al.  Measurement of regional cerebral blood flow in cat brain using intracarotid 2H2O and 2H NMR imaging , 1990, Magnetic resonance in medicine.

[55]  D. Alsop,et al.  Blood flow quantification of the human retina with MRI , 2011, NMR in biomedicine.

[56]  Jack L. Lancaster,et al.  CBF changes during brain activation: fMRI vs. PET , 2004, NeuroImage.

[57]  Paul J. Laurienti,et al.  Dietary Caffeine Consumption Modulates fMRI Measures , 2002, NeuroImage.

[58]  Sven Zuehlsdorff,et al.  Estimation of perfusion and arterial transit time in myocardium using free‐breathing myocardial arterial spin labeling with navigator‐echo , 2010, Magnetic resonance in medicine.

[59]  T Sasaki,et al.  Perfusion Imaging of Brain Tumors Using Arterial Spin-Labeling: Correlation with Histopathologic Vascular Density , 2008, American Journal of Neuroradiology.

[60]  Karam Sidaros,et al.  Noninvasive Measurements of Regional Cerebral Perfusion in Preterm and Term Neonates by Magnetic Resonance Arterial Spin Labeling , 2006, Pediatric Research.

[61]  C. Schönfeldt-Lecuona,et al.  Delusional infestation: Neural correlates and antipsychotic therapy investigated by multimodal neuroimaging , 2010, Progress in Neuro-Psychopharmacology and Biological Psychiatry.

[62]  Thomas F. Nugent,et al.  Dynamic mapping of human cortical development during childhood through early adulthood. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[63]  G. Zaharchuk,et al.  Arterial spin-label imaging in patients with normal bolus perfusion-weighted MR imaging findings: pilot identification of the borderzone sign. , 2009, Radiology.

[64]  G. Aguirre,et al.  Experimental Design and the Relative Sensitivity of BOLD and Perfusion fMRI , 2002, NeuroImage.

[65]  Laura M Parkes,et al.  Depressive Disorders : Focally Altered Cerebral Perfusion Measured with Arterial Spin-labeling MR Imaging 1 , 2009 .

[66]  Weiying Dai,et al.  Modified pulsed continuous arterial spin labeling for labeling of a single artery , 2010, Magnetic resonance in medicine.

[67]  D. S. Williams,et al.  Magnetic resonance imaging of perfusion using spin inversion of arterial water. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[68]  Todd B. Parrish,et al.  Caffeine dose effect on activation-induced BOLD and CBF responses , 2009, NeuroImage.

[69]  Eric C Wong,et al.  Vessel‐encoded arterial spin‐labeling using pseudocontinuous tagging , 2007, Magnetic resonance in medicine.

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

[71]  J. Detre,et al.  Structural MRI of carotid artery atherosclerotic lesion burden and characterization of hemispheric cerebral blood flow before and after carotid endarterectomy , 2006, NMR in biomedicine.

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

[73]  J. Detre,et al.  Noninvasive magnetic resonance imaging evaluation of cerebral blood flow with acetazolamide challenge in patients with cerebrovascular stenosis , 1999, Journal of magnetic resonance imaging : JMRI.

[74]  David C. Alsop,et al.  Assessment of functional development in normal infant brain using arterial spin labeled perfusion MRI , 2008, NeuroImage.

[75]  J. Detre,et al.  Arterial spin labeling perfusion MRI in pediatric arterial ischemic stroke: Initial experiences , 2009, Journal of magnetic resonance imaging : JMRI.

[76]  A. Nobre,et al.  Qualitative mapping of cerebral blood flow and functional localization with echo-planar MR imaging and signal targeting with alternating radio frequency. , 1994, Radiology.

[77]  J. Hendrikse,et al.  Noninvasive MR imaging of cerebral perfusion in patients with a carotid artery stenosis , 2009, Neurology.

[78]  Joseph A Maldjian,et al.  Continuous Arterial Spin Labeled Perfusion Magnetic Resonance Imaging in Patients before and after Carotid Endarterectomy , 2004, Journal of neuroimaging : official journal of the American Society of Neuroimaging.

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

[80]  Anna Rose Childress,et al.  DAT Genotype Modulates Brain and Behavioral Responses Elicited by Cigarette Cues , 2009, Neuropsychopharmacology.

[81]  J A Maldjian,et al.  Detection of mesial temporal lobe hypoperfusion in patients with temporal lobe epilepsy by use of arterial spin labeled perfusion MR imaging. , 2001, AJNR. American journal of neuroradiology.

[82]  Xavier Golay,et al.  Sickle cell disease: continuous arterial spin-labeling perfusion MR imaging in children. , 2003, Radiology.

[83]  Kim Mouridsen,et al.  The QUASAR reproducibility study, Part II: Results from a multi-center Arterial Spin Labeling test–retest study , 2010, NeuroImage.

[84]  Jeroen van der Grond,et al.  Internal carotid artery occlusion assessed at pulsed arterial spin-labeling perfusion MR imaging at multiple delay times. , 2004, Radiology.

[85]  Guillaume Duhamel,et al.  Evaluation of systematic quantification errors in velocity‐selective arterial spin labeling of the brain , 2003, Magnetic resonance in medicine.

[86]  Jeff Duyn,et al.  H215O PET validation of steady‐state arterial spin tagging cerebral blood flow measurements in humans , 2000, Magnetic resonance in medicine.

[87]  J. Detre,et al.  Pediatric perfusion imaging using pulsed arterial spin labeling , 2003, Journal of magnetic resonance imaging : JMRI.

[88]  R R Edelman,et al.  Clinical Outcome in Ischemic Stroke Predicted by Early Diffusion-Weighted and Perfusion Magnetic Resonance Imaging: A Preliminary Analysis , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[89]  John A. Detre,et al.  Serotonin transporter genotype modulates the association between depressive symptoms and amygdala activity among psychiatrically healthy adults , 2011, Psychiatry Research: Neuroimaging.

[90]  R. Ehrman,et al.  Modulation of resting brain cerebral blood flow by the GABA B agonist, baclofen: a longitudinal perfusion fMRI study. , 2011, Drug and alcohol dependence.

[91]  I. Zimine,et al.  Territorial Arterial Spin Labeling in the Assessment of Collateral Circulation: Comparison With Digital Subtraction Angiography , 2008, Stroke.

[92]  M. Zilbovicius,et al.  Changes in regional cerebral blood flow during brain maturation in children and adolescents. , 1992, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[93]  Hengyi Rao,et al.  Serotonin transporter genotype modulates amygdala activity during mood regulation. , 2010, Social cognitive and affective neuroscience.

[94]  M. Tosetti,et al.  Age dependence of cerebral perfusion assessed by magnetic resonance continuous arterial spin labeling , 2007, Journal of magnetic resonance imaging : JMRI.

[95]  J. Trojanowski,et al.  Distinct cerebral perfusion patterns in FTLD and AD , 2010, Neurology.

[96]  I. Christie,et al.  Heightened Resting Neural Activity Predicts Exaggerated Stressor-Evoked Blood Pressure Reactivity , 2009, Hypertension.

[97]  J. Detre,et al.  Reduced Transit-Time Sensitivity in Noninvasive Magnetic Resonance Imaging of Human Cerebral Blood Flow , 1996, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[98]  Wen-Chau Wu,et al.  Quantification Issues in Arterial Spin Labeling Perfusion Magnetic Resonance Imaging , 2010, Topics in magnetic resonance imaging : TMRI.

[99]  Seong-Gi Kim Quantification of relative cerebral blood flow change by flow‐sensitive alternating inversion recovery (FAIR) technique: Application to functional mapping , 1995, Magnetic resonance in medicine.

[100]  Ivan Pedrosa,et al.  Magnetic Resonance Imaging–Measured Blood Flow Change after Antiangiogenic Therapy with PTK787/ZK 222584 Correlates with Clinical Outcome in Metastatic Renal Cell Carcinoma , 2008, Clinical Cancer Research.

[101]  D. Gusnard,et al.  Quantification of Indirect Pathway Inhibition by the Adenosine A2a Antagonist SYN115 in Parkinson Disease , 2010, The Journal of Neuroscience.

[102]  Thomas T. Liu,et al.  Caffeine reduces the activation extent and contrast-to-noise ratio of the functional cerebral blood flow response but not the BOLD response , 2008, NeuroImage.

[103]  J. Hendrikse,et al.  Arterial Spin-Labeling MR Imaging Measurements of Timing Parameters in Patients with a Carotid Artery Occlusion , 2008, American Journal of Neuroradiology.

[104]  Esben Thade Petersen,et al.  Cerebral border zones between distal end branches of intracranial arteries: MR imaging. , 2008, Radiology.

[105]  J. Detre,et al.  Grading of CNS neoplasms using continuous arterial spin labeled perfusion MR imaging at 3 Tesla , 2005, Journal of magnetic resonance imaging : JMRI.

[106]  G. Bruce Pike,et al.  Cerebral Blood Flow Measurement Using fMRI and PET: A Cross-Validation Study , 2008, Int. J. Biomed. Imaging.

[107]  T. L. Davis,et al.  Calibrated functional MRI: mapping the dynamics of oxidative metabolism. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[108]  Seong-Gi Kim,et al.  Early Temporal Characteristics of Cerebral Blood Flow and Deoxyhemoglobin Changes during Somatosensory Stimulation , 2000, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[109]  A J Nederveen,et al.  Acquisition Time and Reproducibility of Continuous Arterial Spin-Labeling Perfusion Imaging at 3T , 2009, American Journal of Neuroradiology.

[110]  M. Raichle The Brain's Dark Energy , 2006, Science.

[111]  Norbert Schuff,et al.  ASL Perfusion MRI Predicts Cognitive Decline and Conversion From MCI to Dementia , 2010, Alzheimer disease and associated disorders.

[112]  Hiroshi Fukuda,et al.  Correlation between gray matter density‐adjusted brain perfusion and age using brain MR images of 202 healthy children , 2011, Human brain mapping.

[113]  Gil Wernovsky,et al.  Preoperative cerebral blood flow is diminished in neonates with severe congenital heart defects. , 2004, The Journal of thoracic and cardiovascular surgery.

[114]  P. Jezzard,et al.  Multiple Inflow Pulsed Arterial Spin-Labeling Reveals Delays in the Arterial Arrival Time in Minor Stroke and Transient Ischemic Attack , 2010, American Journal of Neuroradiology.

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

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

[117]  Britton Chance,et al.  Concurrent measurements of cerebral blood flow, sodium, lactate, and high‐energy phosphate metabolism using 19F, 23Na, 1H, and 31P nuclear magnetic resonance spectroscopy , 1988, Magnetic resonance in medicine.

[118]  John A. Detre,et al.  Using perfusion fMRI to measure continuous changes in neural activity with learning , 2006, Brain and Cognition.

[119]  Angela Hoang,et al.  Minimizing acquisition time of arterial spin labeling at 3T , 2008, Magnetic resonance in medicine.

[120]  A. Federspiel,et al.  Interictal arterial spin-labeling MRI perfusion in intractable epilepsy. , 2010, Journal of neuroradiology. Journal de neuroradiologie.

[121]  D. Gitelman,et al.  On the Use of Caffeine as a Contrast Booster for BOLD fMRI Studies , 2002, NeuroImage.

[122]  Esben Thade Petersen,et al.  Model‐free arterial spin labeling quantification approach for perfusion MRI , 2006, Magnetic resonance in medicine.

[123]  David A. Boas,et al.  A temporal comparison of BOLD, ASL, and NIRS hemodynamic responses to motor stimuli in adult humans , 2006, NeuroImage.

[124]  R. Kraft,et al.  Migraine Associated Cerebral Hyperperfusion with Arterial Spin-Labeled MR Imaging , 2008, American Journal of Neuroradiology.

[125]  J. Detre,et al.  Neural Substrates of Abstinence-Induced Cigarette Cravings in Chronic Smokers , 2007, The Journal of Neuroscience.

[126]  P. Jannin,et al.  Chronic and treatment-resistant depression: A study using arterial spin labeling perfusion MRI at 3Tesla , 2010, Psychiatry Research: Neuroimaging.

[127]  E. Naumann,et al.  Latent state–trait structure of cerebral blood flow in a resting state , 2009, Biological Psychology.

[128]  B. Abler,et al.  Habitual emotion regulation strategies and baseline brain perfusion , 2008, Neuroreport.

[129]  Xavier Golay,et al.  Non-invasive visualization of collateral blood flow patterns of the circle of Willis by dynamic MR angiography , 2006, Medical Image Anal..