Correlation of rapid changes in the average water diffusion constant and the concentrations of lactate and ATP breakdown products during global ischemia in cat brain

Rapid changes in the average water diffusion constant, Dav = 1/3{Dxx + Dyy + Dzz}, and in the concentrations of lactate and purine nucleotides and nucleosides were measured upon global ischemia (cardiac arrest) in cat brain, at a combined time resolution of 36 s (n = 7). At this time resolution, the normalized time curves of 1 ‐ Dav and the increases in ATP breakdown products did not coincide, with the changes in Dav being most rapid. The normalized curves of 1 ‐ Dav and the lactate increase coincided for the first 2‐2.5 min after which the change in Dav was more rapid. After this time point, an excellent correlation was found between the drop in Dav and the decrease in energy utilization rate, which was calculated from the measured time curves of lactate formation and ATP breakdown, and from the time curve for phosphocreatine use reported in the literature. These results are in agreement with the expected biphasic changes in ion and water homeostasis during ischemia and with the model of diffusional changes being a consequence of a water shift from interstitial to intra‐cellular space.

[1]  O. H. Lowry,et al.  EFFECT OF ISCHEMIA ON KNOWN SUBSTRATES AND COFACTORS OF THE GLYCOLYTIC PATHWAY IN BRAIN. , 1964, The Journal of biological chemistry.

[2]  J. Kucharczyk,et al.  Early detection of regional cerebral ischemia in cats: Comparison of diffusion‐ and T2‐weighted MRI and spectroscopy , 1990, Magnetic resonance in medicine.

[3]  P. V. van Zijl,et al.  In situ changes in purine nucleotide and n‐acetyl concentrations upon inducing global ischemia in cat brain , 1993, Magnetic resonance in medicine.

[4]  P van Gelderen,et al.  Water diffusion and acute stroke , 1994, Magnetic resonance in medicine.

[5]  L. Hedlund,et al.  Pre‐ and postmortem diffusion coefficients in rat neural and muscle tissues , 1991, Magnetic resonance in medicine.

[6]  J H Duyn,et al.  Multisection proton MR spectroscopic imaging of the brain. , 1993, Radiology.

[7]  S. Williams,et al.  Diffusion‐Weighted Imaging Studies of Cerebral Ischemia in Gerbils: Potential Relevance to Energy Failure , 1992, Stroke.

[8]  C T Moonen,et al.  Short echo time proton MR spectroscopic imaging. , 1993, Journal of computer assisted tomography.

[9]  J. Kurhanewicz,et al.  Diffusion-weighted MR imaging of acute stroke: correlation with T2-weighted and magnetic susceptibility-enhanced MR imaging in cats. , 1990, AJNR. American journal of neuroradiology.

[10]  J. E. Tanner,et al.  Spin diffusion measurements : spin echoes in the presence of a time-dependent field gradient , 1965 .

[11]  J. Gore,et al.  Changes in water diffusion and relaxation properties of rat cerebrum during status epilepticus , 1993, Magnetic resonance in medicine.

[12]  P. Grenier,et al.  MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. , 1986, Radiology.

[13]  Matthias Fischer,et al.  NMR Imaging of the Apparent Diffusion Coefficient (ADC) for the Evaluation of Metabolic Suppression and Recovery after Prolonged Cerebral Ischemia , 1994, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[14]  B. Siesjö.  Pathophysiology and treatment of focal cerebral ischemia. Part II: Mechanisms of damage and treatment. , 1992, Journal of neurosurgery.

[15]  K. Hossmann,et al.  Diffusion nuclear magnetic resonance imaging in experimental stroke. Correlation with cerebral metabolites. , 1994, Stroke.

[16]  J. Kucharczyk,et al.  Diffusion-Weighted Magnetic Resonance Imaging of Acute Focal Cerebral Ischemia: Comparison of Signal Intensity with Changes in Brain Water and Na+,K+ -ATPase Activity , 1994, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[17]  D. Shungu,et al.  Sensitivity and localization enhancement in multinuclear in vivo NMR spectroscopy by outer volume presaturation , 1993, Magnetic resonance in medicine.

[18]  P. V. van Zijl,et al.  High field localized proton spectroscopy in small volumes: greatly improved localization and shimming using shielded strong gradients , 1989, Magnetic resonance in medicine.

[19]  A. Hansen,et al.  Extracellular ion concentrations during spreading depression and ischemia in the rat brain cortex. , 1981, Acta physiologica Scandinavica.

[20]  K Minematsu,et al.  Diffusion‐weighted magnetic resonance imaging , 1992, Neurology.

[21]  A. van Harreveld,et al.  Changes in cortical extracellular space during spreading depression investigated with the electron microscope. , 1967, Journal of neurophysiology.

[22]  A. Laptook,et al.  Energy Reserves and Utilization Rates in Developing Brain Measured in vivo by 31P and 1H Nuclear Magnetic Resonance Spectroscopy , 1993, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[23]  R Turner,et al.  MR of diffusion slowing in global cerebral ischemia. , 1993, AJNR. American journal of neuroradiology.

[24]  B. Siesjö,et al.  Rate of energy utilization in the cerebral cortex of rats. , 1975, Acta physiologica Scandinavica.

[25]  P van Gelderen,et al.  Restricted and anisotropic displacement of water in healthy cat brain and in stroke studied by NMR diffusion imaging , 1991, Magnetic resonance in medicine.

[26]  C T Moonen,et al.  On the precision of diffusion/perfusion imaging by gradient sensitization , 1992, Magnetic resonance in medicine.

[27]  D Le Bihan,et al.  Measuring random microscopic motion of water in tissues with MR imaging: a cat brain study. , 1991, Journal of computer assisted tomography.

[28]  Chrit T. W. Moonen,et al.  Diffusion Spectroscopy in Living Systems , 1994 .

[29]  Chrit T. W. Moonen,et al.  Highly Effective Water Suppression for in vivo proton NMR Spectroscopy (DRYSTEAM) , 1990 .

[30]  J. Ulatowski,et al.  Rapid monitoring of changes in water diffusion coefficients during reversible ischemia in cat and rat brain , 1994, Magnetic resonance in medicine.

[31]  K. Hossmann,et al.  NMR Spectroscopic Investigation of the Recovery of Energy and Acid—Base Homeostasis in the Cat Brain after Prolonged Ischemia , 1989, Journal of cerebral blood flow and metabolism : official journal of the International Society of Cerebral Blood Flow and Metabolism.

[32]  J. Frahm,et al.  Diffusion imaging of the human brain in vivo using high‐speed STEAM MRI , 1992, Magnetic resonance in medicine.

[33]  Wei Li,et al.  Fast magnetic resonance diffusion‐weighted imaging of acute human stroke , 1992, Neurology.

[34]  K Minematsu,et al.  Reversible Focal Ischemic Injury Demonstrated by Diffusion‐Weighted Magnetic Resonance Imaging in Rats , 1992, Stroke.

[35]  R N Bryan,et al.  Sodium, ATP, and intracellular pH transients during reversible complete ischemia of dog cerebrum. , 1991, Stroke.

[36]  Jens Frahm,et al.  Localized proton spectroscopy using stimulated echoes. , 1987 .

[37]  R A Knight,et al.  Temporal evolution of ischemic damage in rat brain measured by proton nuclear magnetic resonance imaging. , 1991, Stroke.

[38]  P. V. van Zijl,et al.  Diffusion Weighting by the Trace of the Diffusion Tensor within a Single Scan , 1995, Magnetic resonance in medicine.

[39]  L. Hedlund,et al.  Mechanism of Detection of Acute Cerebral Ischemia in Rats by Diffusion‐Weighted Magnetic Resonance Microscopy , 1992, Stroke.

[40]  A. Hansen,et al.  Brain extracellular space during spreading depression and ischemia. , 1980, Acta physiologica Scandinavica.

[41]  K. Hossmann,et al.  PURINE NUCLEOTIDE METABOLISM IN THE CAT BRAIN AFTER ONE HOUR OF COMPLETE ISCHEMIA , 1974, Journal of neurochemistry.

[42]  C. Sotak,et al.  Spreading waves of decreased diffusion coefficient lifter cortical stimulation in the rat brain , 1994, Magnetic resonance in medicine.

[43]  P. V. van Zijl,et al.  Evaluation of restricted diffusion in cylinders. Phosphocreatine in rabbit leg muscle. , 1994, Journal of magnetic resonance. Series B.

[44]  I. Silver,et al.  Ions and energy in mammalian brain , 1994, Progress in Neurobiology.

[45]  P. Basser,et al.  MR diffusion tensor spectroscopy and imaging. , 1994, Biophysical journal.

[46]  G Di Chiro,et al.  Histopathologic correlates of abnormal water diffusion in cerebral ischemia: diffusion-weighted MR imaging and light and electron microscopic study. , 1993, Radiology.

[47]  R G Shulman,et al.  High-resolution 1H nuclear magnetic resonance study of cerebral hypoxia in vivo. , 1983, Proceedings of the National Academy of Sciences of the United States of America.