Feasibility of mapping the tissue mass corrected bioscale of cerebral metabolic rate of oxygen consumption using 17-oxygen and 23-sodium MR imaging in a human brain at 9.4T

The reduction of molecular oxygen to water is the final step of oxidative phosphorylation that couples adenosine triphosphate production to the reoxidation of reducing equivalents formed during the oxidation of glucose to carbon dioxide. This coupling makes the cerebral metabolic rate of oxygen consumption (CMRO(2)) an excellent reflection of the metabolic health of the brain. A multi-nuclear magnetic resonance (MR) imaging based method for CMRO(2) mapping is proposed. Oxygen consumption is determined by applying a new three-phase metabolic model for water generation and clearance to the changing 17-oxygen ((17)O) labeled water MR signal measured using quantitative (17)O MR imaging during inhalation of (17)O-enriched oxygen gas. These CMRO(2) data are corrected for the regional brain tissue mass computed from quantitative 23-sodium MR imaging of endogenous tissue sodium ions to derive quantitative results of oxygen consumption in micromoles O(2)/g tissue/minute that agree with literature results reported from positron emission tomography. The proposed technique is demonstrated in the human brain using a 9.4 T MR scanner optimized for human brain imaging.

[1]  M. Alexander,et al.  Principles of Neural Science , 1981 .

[2]  S. Kety,et al.  THE NITROUS OXIDE METHOD FOR THE QUANTITATIVE DETERMINATION OF CEREBRAL BLOOD FLOW IN MAN: THEORY, PROCEDURE AND NORMAL VALUES. , 1948, The Journal of clinical investigation.

[3]  Charles S Springer,et al.  Equilibrium water exchange between the intra‐ and extracellular spaces of mammalian brain , 2003, Magnetic resonance in medicine.

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

[5]  Peter T Fox,et al.  Quantitative measurement of oxygen metabolic rate in the rat brain using microPET imaging of briefly inhaled 15O-labelled oxygen gas , 2006, Nuclear medicine communications.

[6]  Watabe Hiroshi,et al.  Rapid protocol for quantitative CMRO2 and CBF using PET and O-15 labelled compounds , 2004 .

[7]  K. Ishii,et al.  Changes in cerebral blood flow and oxygen metabolism related to magnetic resonance imaging white matter hyperintensities in Alzheimer's disease. , 1997, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[8]  M E Raichle,et al.  Measurement of brain oxygen utilization with radioactive oxygen-15: experimental verification. , 1976, Journal of applied physiology.

[9]  Yi Zhang,et al.  Erratum: Development of 17O NMR approach for fast imaging of cerebral metabolic rate of oxygen in rat brain at high field (Proceedings of the National Academy of Sciences of the United States (October 1, 2002) 99:20 (13194-13199)) , 2003 .

[10]  Nadim Joni Shah,et al.  Fast quantitative mapping of absolute water content with full brain coverage , 2008, NeuroImage.

[11]  Kamil Ugurbil,et al.  Development of 17O NMR approach for fast imaging of cerebral metabolic rate of oxygen in rat brain at high field , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[12]  G B Drummond,et al.  Systemic recirculation assessed in apnoeic anaesthetized patients using carbon dioxide concentration measurements during stepwise expiration. , 2009, British journal of anaesthesia.

[13]  K. Jamrozik,et al.  Incidence and outcome of cerebrovascular disease in Perth, Western Australia. , 1988, Stroke.

[14]  M E Raichle,et al.  Evidence of the Limitations of Water as a Freely Diffusible Tracer in Brain of the Rhesus Monkey , 1974, Circulation research.

[15]  J. Pekar,et al.  In Vivo measurement of cerebral oxygen consumption and blood flow using 17O magnetic resonance imaging , 1991, Magnetic resonance in medicine.

[16]  Keith R Thulborn,et al.  Absolute molar concentrations by NMR in inhomogeneous B1. A scheme for analysis of in vivo metabolites , 1983 .

[17]  S Wing,et al.  Stroke mortality maps. United States whites aged 35-74 years, 1962-1982. , 1988, Stroke.

[18]  R. W. McGilvery,et al.  Biochemistry, a functional approach , 1979 .

[19]  J. Kirk,et al.  A rapid titrimetric method for determining the water content of human blood. , 1953, Science.

[20]  George G. Somjen,et al.  Ions in the Brain: Normal Function, Seizures, and Stroke , 2004 .

[21]  Ole Henriksen,et al.  Indicator Methods for Measurement of Organ and Tissue Blood Flow , 2011 .

[22]  C. Nicholson,et al.  Diffusion in brain extracellular space. , 2008, Physiological reviews.

[23]  Aiming Lu,et al.  Quantitative sodium imaging with a flexible twisted projection pulse sequence , 2010, Magnetic resonance in medicine.

[24]  Meir H. Kryger Pathophysiology of respiration , 1981 .

[25]  Janusz Hankiewicz,et al.  17O magnetic resonance imaging of the human brain , 2004, Neurological research.

[26]  G. D. Mateescu,et al.  Concerted Oxygen-17/Phosphorus-31 Magnetic Resonance Spectroscopy: A Novel Approach for In Vivo Correlation of Oxygen Consumption and Phosphate Metabolism , 1994 .

[27]  J. Brandt,et al.  Regional hypometabolism in Alzheimer's disease as measured by positron emission tomography after correction for effects of partial volume averaging , 1996, Neurology.

[28]  M J Welch,et al.  The measure in vivo of regional cerebral oxygen utilization by means of oxyhemoglobin labeled with radioactive oxygen-15. , 1970, The Journal of clinical investigation.

[29]  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.

[30]  G. Lapin,et al.  Microvessel organization and structure in experimental brain tumors: microvessel populations with distinctive structural and functional properties. , 1999, Microvascular research.

[31]  A. Nier,et al.  A Redetermination of the Relative Abundances of the Isotopes of Carbon, Nitrogen, Oxygen, Argon, and Potassium , 1950 .

[32]  William J Powers,et al.  Variability of cerebral blood volume and oxygen extraction: stages of cerebral haemodynamic impairment revisited. , 2002, Brain : a journal of neurology.

[33]  K R Thulborn,et al.  Quantitative tissue sodium concentration mapping of the growth of focal cerebral tumors with sodium magnetic resonance imaging , 1999, Magnetic resonance in medicine.

[34]  I. Kanno,et al.  Arterial fraction of cerebral blood volume in humans measured by positron emission tomography , 2001, Annals of nuclear medicine.

[35]  K. Ishii,et al.  Decreased medial temporal oxygen metabolism in Alzheimer's disease shown by PET. , 1996, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[36]  W J Powers,et al.  Count-based PET method for predicting ischemic stroke in patients with symptomatic carotid arterial occlusion. , 1999, Radiology.

[37]  D. Fiat,et al.  Determination of the rate of cerebral oxygen consumption and regional cerebral blood flow by non-invasive 17O in vivo NMR spectroscopy and magnetic resonance imaging: Part 1. Theory and data analysis methods. , 1992, Neurological research.

[38]  Cerebrovascular disease mortality and Medicare hospitalization--United States, 1980-1990. , 1992, MMWR. Morbidity and mortality weekly report.

[39]  Yi Zhang,et al.  In vivo 17O NMR approaches for brain study at high field , 2005, NMR in biomedicine.

[40]  M. Mintun,et al.  Brain oxygen utilization measured with O-15 radiotracers and positron emission tomography. , 1984, Journal of nuclear medicine : official publication, Society of Nuclear Medicine.

[41]  M Dujovny,et al.  Determination of regional cerebral oxygen consumption in the human: 17O natural abundance cerebral magnetic resonance imaging and spectroscopy in a whole body system. , 1993, Neurological research.

[42]  Fahmeed Hyder,et al.  A Multiparametric Assessment of Oxygen Efflux from the Brain , 2006, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[43]  F E Boada,et al.  Quantitative tissue sodium concentration mapping of normal rat brain , 1996, Magnetic resonance in medicine.

[44]  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.

[45]  K. Thulborn,et al.  Characterization and correction of system delays and eddy currents for MR imaging with ultrashort echo‐time and time‐varying gradients , 2009, Magnetic resonance in medicine.

[46]  Fahmeed Hyder,et al.  Energetic basis of brain activity: implications for neuroimaging , 2004, Trends in Neurosciences.

[47]  A. Macovski,et al.  Selection of a convolution function for Fourier inversion using gridding [computerised tomography application]. , 1991, IEEE transactions on medical imaging.

[48]  H. Kimelberg Water homeostasis in the brain: Basic concepts , 2004, Neuroscience.

[49]  Scott T. Grafton,et al.  Automated image registration: I. General methods and intrasubject, intramodality validation. , 1998, Journal of computer assisted tomography.

[50]  Peter Herscovitch,et al.  Correction of Positron Emission Tomography Data for Cerebral Atrophy , 1986, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[51]  K. Behar,et al.  Natural abundance (17)O NMR spectroscopy of rat brain in vivo. , 2008, Journal of magnetic resonance.

[52]  Lawrence J. Berliner,et al.  Ultra High Field Magnetic Resonance Imaging , 2006 .

[53]  K. Ishimori,et al.  Cerebral oxygen utilization analyzed by the use of oxygen-17 and its nuclear magnetic resonance. , 1990, Biochemical and biophysical research communications.

[54]  Jiaquan Xu,et al.  Deaths: final data for 2006. , 2009, National vital statistics reports : from the Centers for Disease Control and Prevention, National Center for Health Statistics, National Vital Statistics System.

[55]  Kamil Ugurbil,et al.  Simplified Methods for Calculating Cerebral Metabolic Rate of Oxygen Based on 17O Magnetic Resonance Spectroscopic Imaging Measurement during a Short 17O2 Inhalation , 2004, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.