Correlation of early reduction in the apparent diffusion coefficient of water with blood flow reduction during middle cerebral artery occlusion in rats
Corresponding Author
Anthony Mancuso PhD
Departments of Neurological Surgery, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
MRI Unit 114M, VA Medical Center, 4150 Clement St., San Francisco, CA 94121===Search for more papers by this authorHiroshi Karibe
Departments of Neurological Surgery, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Departments of Neurological Surgery, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Search for more papers by this authorWilliam D. Rooney
Radiology, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Departments of Neurological Surgery, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Search for more papers by this authorGregory J. Zarow
Departments of Neurological Surgery, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Departments of Neurological Surgery, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Search for more papers by this authorSteven H. Graham
Neurology, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Departments of Neurological Surgery, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Search for more papers by this authorMichael W. Weiner
Radiology, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Departments of Neurological Surgery, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Search for more papers by this authorPhilip R. Weinstein
Medicine, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California.
Departments of Neurological Surgery, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Search for more papers by this authorCorresponding Author
Anthony Mancuso PhD
Departments of Neurological Surgery, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
MRI Unit 114M, VA Medical Center, 4150 Clement St., San Francisco, CA 94121===Search for more papers by this authorHiroshi Karibe
Departments of Neurological Surgery, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Departments of Neurological Surgery, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Search for more papers by this authorWilliam D. Rooney
Radiology, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Departments of Neurological Surgery, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Search for more papers by this authorGregory J. Zarow
Departments of Neurological Surgery, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Departments of Neurological Surgery, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Search for more papers by this authorSteven H. Graham
Neurology, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Departments of Neurological Surgery, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Search for more papers by this authorMichael W. Weiner
Radiology, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Departments of Neurological Surgery, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Search for more papers by this authorPhilip R. Weinstein
Medicine, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California.
Departments of Neurological Surgery, Veterans Administration Medical Center and School of Medicine, University of California, San Francisco, California
Search for more papers by this authorAbstract
To determine the relationship between reductions in the apparent diffusion coefficient of water (ADC) and in cerebral blood flow (CBF) during focal ischemia, we used diffusion-weighted magnetic resonance (D-MR) imaging and autoradiographic CBF analysis to examine rats subjected to 30 or 90 min of permanent middle cerebral artery (MCA) occlusion. In the 30-min occlusion group (n = 10), the area with substantially reduced ADC (15% or more below the contralateral level [ADC15]) corresponded best to the area with CBF below 25 ml/100 g/min and was significantly smaller than the area with CBF below 50 ml/100 g/min (CBF50), a level associated with reduced protein synthesis and delayed necrosis (40 ± 13% versus 74 ± 8% of the ischemic hemisphere; P < 0.0001). In the 90-min occlusion group (n = 6), the ADC15 area corresponded best to the CBF30 to CBF35 area and was again significantly smaller than the CBF50 area (54 ± 13% versus 73 ± 20%, P < 0.05). Thus, the area of substantially reduced ADC at 30 and 90 min represents only 53% and 74%, respectively, of the tissue at risk for infarction. These findings indicate a potential limitation in using early D-MR imaging to predict stroke outcome.
Reference
- 1 M. E. Moseley, J. Kucharczyk, J. Mintorovitch, Y. Cohen, J. Kurhanewicz, N. Derugin, H. Asgari, D. Norman, Diffusion-weighted MR imaging of acute stroke: correlation with T2-weighted and magnetic susceptibility-enhanced MR imaging in cats. AJNR. Am. J. Neuroradiol. 11, 423–429 (1990).
- 2 M. E. Moseley, Y. Cohen, J. Mintorovitch, L. Chileuitt, H. Shimizu, J. Kucharczyk, M. F. Wendland, P. R. Weinstein, Early detection of regional cerebral ischemia in cats: comparison of diffusion- and T2-weighted MRI and spectroscopy. Magn. Reson. Med. 14, 330–346 (1990).
- 3 S. A. Roussel, N. van Bruggen, M. D. King, J. Houseman, S. R. Williams, D. G. Gadian, Monitoring the initial expansion of local ischaemic changes by diffusion-weighted MRI using a remote controlled method of occlusion. NMR Biomed. 7, 21–28 (1994).
- 4 S. Warach, D. Chien, W. Li, M. Ronthal, R. R. Edelman, Fast magnetic resonance diffusion-weighted imaging of acute human stroke. Neurology 42, 1717–1723 (1992). [Published erratum appears in Neurology 1992 Nov; 42 (11), 2192].
- 5 J. Zhong, O. A. Petroff, J. W. Prichard, J. C. Gore, Changes in water diffusion and relaxation properties of rat cerebrum during status epilepticus. Magn. Reson. Med. 30, 241–246 (1993).
- 6 L. L. Latour, Y. Hasegawa, J. E. Formato, M. Fisher, C. H. Sotak, Spreading waves of decreased diffusion coefficient after cortical stimulation in the rat brain. Magn. Reson. Med. 32, 189–198 (1994).
- 7 H. Benveniste, L. W. Hedlund, G. A. Johnson, Mechanism of detection of acute cerebral ischemia in rats by diffusion-weighted magnetic resonance microscopy. Stroke 23, 746–754 (1992).
- 8 M. van Lookeren Campagne, J. B. Verheul, K. Nicolay, R. Balazs. Early evolution and recovery from excitotoxic injury in the neonatal rat brain: a study combining magnetic resonance imaging, electrical impedance, histology. J. Cereb. Blood Flow Metab. 14, 1011–1023 (1994).
- 9 H. B. Verheul, R. Balazs, J. W. Berkelbach van der Sprenkel, C. A. Tulleken, K. Nicolay, K. S. Tamminga, M. van Lookeren Campagne, Comparison of diffusion-weighted MRI with changes in cell volume in a rat model of brain injury. NMR. Biomed. 7, 96–100 (1994).
- 10 D. G. Norris, T. Niendorf, D. Leibfritz, Healthy and infarcted brain tissues studied at short diffusion times: the origins of apparent restriction and the reduction in apparent diffusion coefficient. NMR Biomed. 7, 304–310 (1994).
- 11 A. Bizzi, A. Righini, R. Turner, D. LeBihan, D. DesPres, G. Di Chiro, J. R. Alger, MR of diffusion slowing in global cerebral ischemia. AJNR. Am. J. Neuroradiol. 14, 1347–1354 (1993).
- 12 J. Mintorovitch, M. E. Moseley, L. Chileuitt, H. Shimizu, Y. Cohen, P. R. Weinstein, Comparison of diffusion- and T2-weighted MRI for the early detection of cerebral ischemia and reperfusion in rats. Magn. Reson. Med. 18, 39–50 (1991).
- 13 P. van Gelderen, M. H. de Vleeschouwer, D. DesPres, J. Pekar, P. C. van Zijl, C. T. Moonen, Water diffusion and acute stroke. Magn. Reson. Med. 31, 154–163 (1994).
- 14 D. Davis, J. Ulatowski, S. Eleff, M. Izuta, S. Mori, D. Shungu, P. C. van Zijl, Rapid monitoring of changes in water diffusion coefficients during reversible ischemia in cat and rat brain. Magn. Reson. Med. 31, 454–460 (1994).
- 15 J. Mintorovitch, G. Y. Yang, H. Shimizu, J. Kucharczyk, P. H. Chan, P. R. Weinstein. Diffusion-weighted magnetic resonance imaging of acute focal cerebral ischemia: comparison of signal intensity with changes in brain water and Na+,K +-ATPase activity. J. Cereb. Blood Flow Metab. 14, 332–336 (1994).
- 16 G. Mies, S. Ishimaru, Y. Xie, K. Seo, K. A. Hossmann, Ischemic thresholds of cerebral protein synthesis and energy state following middle cerebral artery occlusion in rat. J. Cereb. Blood Flow Metab. 11, 753–761 (1991).
- 17 K. A. Hossmann, Viability thresholds and the penumbra of focal ischemia. Ann. Neurol. 36, 557–565 (1994).
- 18 K. Takagi, M. D. Ginsberg, M. Y. Globus, W. D. Dietrich, E. Martinez, S. Kraydieh, R. Busto, Changes in amino acid neurotransmitters and cerebral blood flow in the ischemic penumbral region following middle cerebral artery occlusion in the rat: correlation with histopathology. J. Cereb. Blood Flow Metab. 13, 575–585 (1993).
- 19 A. Tamura, D. I. Graham, J. McCulloch, G. M. Teasdale, Focal cerebral ischaemia in the rat: 2. Regional cerebral blood flow determined by [14C]iodoantipyrine autoradiography following middle cerebral artery occlusion. J. Cereb. Blood Flow Metab. 1, 61–69 (1981).
- 20 M. Jacewicz, J. Tanabe, W. A. Pulsinelli, The CBF threshold and dynamics for focal cerebral infarction in spontaneously hypertensive rats. J. Cereb. Blood Flow Metab. 12, 359–370 (1992).
- 21 H. Karibe, J. Chen, G. J. Zarow, S. H. Graham, P. R. Weinstein, Delayed induction of mild hypothermia to reduce infarct volume after temporary middle cerebral artery occlusion in rats. J. Neurosurg. 80, 112–119 (1994).
- 22 J. Chen, G. J. Zarow, S. H. Graham, P. R. Weinstein, Duration threshold of ischema for early reperfusion injury in reversible focal ischemia in rats. Stroke 22, 127 (1991) [Abstract].
- 23 E. O. Stejskal, J. E. Tanner, Spin diffusion measurements: spin-echoes in the presence of a time dependent field gradient. J. Chem. Phys. 42, 288–292 (1965).
- 24 D. Le Bihan, E. Breton, D. Lallemand, P. Grenier, E. Cabanis, M. Laval-Jeantet, MR imaging of intravoxel incoherent motions: application to diffusion and perfusion in neurologic disorders. Radiology 161, 401–407 (1986).
- 25 T. M. Jay, G. Lucignani, A. M. Crane, J. Jehle, L. Sokoloff, Measurement of local cerebral blood flow with [14C]iodoantipyrine in the mouse. J. Cereb. Blood Flow Metab. 8, 121–129 (1988).
- 26 L. D. Fischer, G. van Belle, “ Biostatistics: A Methodology for the Health Sciences,” John Wiley & Sons, New York, 1993.
- 27 M. Nedergaard, N. H. Diemer. Focal ischemia of the rat brain, with special reference to the influence of plasma glucose concentration. Acta Neuropathol. (Berl) 73, 131–137 (1987).
- 28 T. Maekawa, C. Tommasino, H. M. Shapiro, J. Keifer-Good-man, R. W. Kohlenberger, Local cerebral blood flow and glucose utilization during isoflurane anesthesia in the rat. Anesthesiology 65, 144–151 (1986).
- 29 S. Ogawa, T. M. Lee, A. S. Nayak, P. Glynn, Oxygenation-sensitive contrast in magnetic resonance image of rodent brain at high magnetic fields. Magn. Reson. Med. 14, 68–78 (1990).
- 30 B. K. Siesjo, Pathophysiology and treatment of focal cerebral ischemia. Part I: Pathophysiology. J. Neurosurg. 77, 169–184 (1992).
- 31 Y. Hasegawa, M. Fisher, L. L. Latour, B. J. Dardzinski, C. H. Sotak, MRI diffusion mapping of reversible and irreversible ischemic injury in focal brain ischemia. Neurology 44, 1484–1490 (1994).
- 32 M. E. Moseley, J. Kucharczyk, H. S. Asgari, D. Norman, Anisotropy in diffusion-weighted MRI. Magn. Reson. Med. 19, 321–326 (1991).
- 33 G. Fox, D. Gallacher, S. Shevde, J. Loftus, G. Swayne, Anatomic variation of the middle cerebral artery in the Sprague-Dawley rat. Stroke 24, 2087–92 (1993).
- 34 Q. Jiang, Z. G. Zhang, M. Chopp, J. A. Helpern, R. J. Ordidge, J. H. Garcia, B. A. Marchese, Z. X. Qing, R. A. Knight, Temporal evolution and spatial distribution of the diffusion constant of water in rat brain after transient middle cerebral artery occlusion. J. Neurol. Sci. 120, 123–130 (1993).
- 35 B. J. Dardzinski, C. H. Sotak, M. Fisher, Y. Hasegawa, L. Li, K. Minematsu, Apparent diffusion coefficient mapping of experimental focal cerebral ischemia using diffusion-weighted echo-planar imaging. Magn. Reson. Med. 30, 318–325 (1993).
- 36 A. L. Busza, K. L. Allen, M. D. King, N. van Bruggen, S. R. Williams, D. G. Gadian, Diffusion-weighted imaging studies of cerebral ischemia in gerbils. Potential relevance to energy failure. Stroke 23, 1602–1612 (1992).
- 37 M. Hoehn-Berlage, D. Norris, K. Kohno, G. Mies, D. Leibfritz, K. A. Hossman, Early infarct evolution in rat brain: NMR diffusion imaging, regional blood flow, ATP and tissue pH, in “Proc., SMRM, 12th Annual Meeting, 1993” p. 250.
- 38 K. Minematsu, L. Li, M. Fisher, C. H. Sotak, M. A. Davis, M. S. Fiandaca, Diffusion-weighted magnetic resonance imaging: rapid and quantitative detection of focal brain ischemia. Neurology 42, 235–240 (1992).
- 39 M. Nedergaard, A. J. Hansen, Characterization of cortical depolarizations evoked in focal cerebral ischemia. J. Cereb. Blood Flow Metab. 13, 568–574 (1993).
- 40 Y. Hasegawa, L. L. Latour, J. E. Formato, C. H. Sotak, M. Fisher, Spreading waves of a reduced diffusion coefficient of water in normal and ischemic rat brain. J. Cereb. Blood Flow Metab. 15, 179–187 (1995).
- 41 T. P. Roberts, Z. Vexler, N. Derugin, M. E. Moseley, J. Kucharczyk, High-speed MR imaging of ischemic brain injury following stenosis of the middle cerebral artery. J. Cereb. Blood Flow Metab. 13, 940–946 (1993).
