Review Article
The role of diffusion tensor imaging in the evaluation of ischemic brain injury – a review
Article first published online: 5 DEC 2002
DOI: 10.1002/nbm.786
Copyright © 2002 John Wiley & Sons, Ltd.
Issue
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NMR in Biomedicine
Special Issue: Diffusion tensor imaging and axonal mapping - state of the art
Volume 15, Issue 7-8, pages 561–569, November - December 2002
Additional Information
How to Cite
Sotak, C. H. (2002), The role of diffusion tensor imaging in the evaluation of ischemic brain injury – a review. NMR Biomed., 15: 561–569. doi: 10.1002/nbm.786
Publication History
- Issue published online: 5 DEC 2002
- Article first published online: 5 DEC 2002
- Manuscript Revised: 28 NOV 2001
- Manuscript Accepted: 28 NOV 2001
- Manuscript Received: 6 JUN 2001
- Abstract
- Article
- References
- Cited By
Keywords:
- magnetic resonance imaging;
- diffusion imaging;
- diffusion tensor imaging;
- multiparametric magnetic resonance imaging;
- cerebral ischemia;
- water apparent diffusion coefficient;
- diffusion anisotropy
Abstract
Water diffusion in brain tissue is affected by the presence of barriers to translational motion such as cell membranes and myelin fibers. The measured water apparent diffusion coefficient (ADC) value is therefore frequently anisotropic and varies depending upon the orientation of restricting barriers (such as white matter tracts) relative to the diffusion-sensitive-gradient direction. Anisotropic water diffusion can be specified using indices of diffusion anisotropy [e.g. standard deviation of the individual ADC values, fractional anisotropy (FA), lattice index (LI)], which are derived from measurements of the full diffusion tensor. The rotationally invariant nature of particular diffusion anisotropy indices (e.g. FA, LI) allows orientation-independent comparisons of these parameters between different subjects. Pathophysiological processes (such as cerebral ischemia) that modify the integrity of the tissue microstructure result in significant alterations in tissue anisotropy and make this metric a useful endpoint for characterizing the temporal evolution of the disease. Diffusion-tensor imaging (DTI) studies of both experimental and human stroke suggest that DTI may provide additional information about the evolution of the disease that is not available from diffusion-weighted MRI (DWI) alone. Acute reductions in the average diffusivity [<D> = (λ1 + λ2 + λ3)/3 where λ1, λ2, and λ3 are the eigenvalues of the diffusion tensor] following the onset of cerebral ischemia are often accompanied by increases in diffusion anisotropy. In the transition from acute to sub-acute and chronic stroke, <D> renormalizes and subsequently increases whereas diffusion anisotropy measures (e.g. FA) decline and remained reduced in chronic infarcts. Overall isotropic ADC changes during infarct evolution have been observed to be greater in white matter (WM) than in gray matter (GM) lesions (although there have been conflicting reports on this issue) and GM lesions tend to renormalize prior to WM lesions as the infarct evolves. Ischemic WM exhibits a significant decrease in diffusion anisotropy (relative to normal WM) during ischemic evolution whereas that of ischemic GM remains statistically unchanged. Furthermore, the percentage decrease in ischemic WM <D> is largely determined by reductions in λ1, the eigenvalue that coincides with the long axis of the WM fiber tract. Variations in unidirectional ADC or <D> over the ischemic time course limit the usefulness of this parameter alone as a predictor of ischemic injury. Consequently, ADC information has been combined with that of other MR parameters (including DTI) to unambiguously stage and predict ischemic brain injury over its entire temporal evolution. Combined <D> and diffusion anisotropy measurements have identified three phases of diffusion abnormality: (1) reduced <D> and elevated anisotropy; (2) reduced <D> and reduced anisotropy; and (3) elevated <D> and reduced anisotropy. However, variations in the differential patterns of <D> and diffusion anisotropy evolution have been observed by a number of investigators and more work is needed to clarify the role of these measurements in characterizing the severity of the ischemic insult as well as the potential outcome in response to the initial ischemic injury. The use of DTI, in combination with more sophisticated analysis methods for performing multiparametric segmentation, such as multispectral analysis, may enhance the use of MRI for accurate diagnosis and prognosis of stroke. Furthermore, these techniques may also play an important role in the clinical evaluation of new stroke treatments. Copyright © 2002 John Wiley & Sons, Ltd.
REFERENCES
- 1, . Biological differences between ischemia, hypoglycemia and epilepsy. Ann. Neurol. 1987; 24: 699–707.Direct Link:
- 2. Pathophysiological aspects of brain edema. Acta Neuropathol. (Berl.) 1987; 72: 236–239.
- 3, , , , , , . Rapid monitoring of changes in water diffusion coefficients during reversible ischemia in cat and rat brain. Magn. Reson. Med. 1994; 31: 454–460.Direct Link:
- 4, , , , , . Comparison of diffusion- and T2-weighted MRI for the early detection of cerebral ischemia and reperfusion in rats. Magn. Reson. Med. 1991; 18: 39–50.Direct Link:
- 5, , , , , , , . Early detection of regional cerebral ischemia in cats: comparison of diffusion- and T2-weighted MRI and spectroscopy. Magn. Reson. Med. 1990; 14: 330–346.Direct Link:
- 6, , , , , . Diffusion-weighted magnetic resonance imaging: rapid and quantitative detection of focal brain ischemia. Neurology 1992; 42: 235–240.
- 7, , , . Anisotropy in diffusion-weighted MRI. Magn. Reson. Med. 1991; 19: 321–326.Direct Link:
- 8, . MR imaging of anisotropic and restricted diffusion by simultaneous use of spin and stimulated echoes. Magn. Reson. Med. 1992; 26: 174–183.Direct Link:
- 9, , , , , , , , . Effects of diffusion anisotropy on lesion delineation in a rat model of cerebral ischemia. Magn. Reson. Med. 1997; 38: 662–668.Direct Link:
- 10, , . MR diffusion tensor spectroscopy and imaging. Biophys. J. 1994; 66: 259–267.
- 11, , , , , . Water diffusion in acute stroke. Magn. Reson. Med. 1994; 31: 154–163.Direct Link:
- 12, . Single-scan magnetic resonance imaging of the trace of the diffusion tensor. Magn. Reson. Med. 1995; 33: 41–52.Direct Link:
- 13, , . Optimized isotropic diffusion weighting. Magn. Reson. Med. 1995; 34: 139–143.Direct Link:
- 14. Inferring microstructural features and the physiological state of tissues from diffusion-weighted images. NMR Biomed. 1995; 8: 333–344.Direct Link:
- 15, . Toward a quantitative assessment of diffusion anisotropy. Magn. Reson. Med. 1996; 36: 893–906.Direct Link:
- 16, , . Fast tensor imaging of water diffusion changes in gray and white matter following cardiac arrest in cats. Proc. Int. Soc. Magn. Reson. Med. 1996; 3: 314.
- 17, , , , . The temporal evolution of diffusion anisotropy in the ischemic rat brain. Proc. Int. Soc. Magn. Reson. Med. 1998; 5: 530.
- 18, , , , , , . Multispectral analysis of the temporal evolution of cerebral ischemia in the rat brain. J. Magn. Reson. Imag. 2000; 12: 842–858.Direct Link:
- 19, , , . Diffusion anisotropy imaging of stroke. Proc. Int. Soc. Magn. Reson. Med. 1997; 4: 573.
- 20, , , , , . Histopathological correlations of nuclear magnetic resonance imaging parameters in experimental cerebral ischemia. Magn. Reson. Imag. 1993; 11: 241–246.
- 21, , , , . MRI assessment of evolving focal cerebral ischemia: comparison with histopathology in rats. Stroke 1994; 25: 1252–1262.
- 22, , , , , , , , . The temporal evolution of MRI tissue signatures after transient middle cerebral artery occlusion in rat. J. Neurol. Sci. 1997; 145: 15–23.
- 23, , , , , . Identification of fiber degeneration and organized gliosis in stroke patients by diffusion tensor MRI. Proc. Int. Soc. Magn. Reson. Med. 1996; 3: 563.
- 24, , , , , , . The nature of chronic ischaemic damage and lacunar infarction demonstrated by diffusion tensor MRI. Proc. Int. Soc. Magn. Reson. Med. 1997; 3: 1712
- 25, , , , . Acute human stroke studied by whole brain echo planar diffusion-weighted magnetic resonance imaging. Ann. Neurol. 1995; 37: 231–241.Direct Link:
- 26, , , , , . Acute and chronic stroke: navigated spin-echo diffusion-weighted MR imaging. Radiology 1996; 199: 403–408.
- 27, , , , , , , , , , , , , , , , . Hyperacute stroke: evaluation with combined multisection diffusion-weighted and hemodynamically-weighted echo-planar imaging. Radiology 1996; 199: 391–401.
- 28, , , , , , , , , . A model to predict histopathology of human stroke using diffusion and T2-weighted magnetic resonance imaging. Stroke 1995; 26: 1983–1989.
- 29, , , , , . Clinical utility of diffusion-weighted magnetic resonance imaging in the assessment of ischemic stroke. Ann. Neurol. 1997; 41: 574–580.Direct Link:
- 30, , , , , , , , , . Time course of lesion development in patients with acute stroke: serial diffusion- and hemodynamic-weighted magnetic resonance imaging. Stroke 1998; 29: 2268–2276.
- 31, , , , , , , , , . An evaluation of the time dependence of the anisotropy of the water diffusion tensor in acute human stroke. Magn. Reson. lmag. 1999; 17: 331–348.
- 32, , , , , , , . Serial study of apparent diffusion coefficient and anisotropy in patients with acute stroke. Stroke 1999; 30: 2382–2390.
- 33, , , , , , . Diffusion tensor imaging can detect and quantify corticospinal tract degeneration after stroke. J. Neurol. Neurosurg. Psychiat. 2000; 69: 269–272.
- 34, , , . Time course of diffusion imaging abnormalities in human stroke. Stroke 1996; 27: 1254–1256.
- 35, , . Pitfalls and potential of clinical diffusion-weighted MR imaging in acute stroke. Stroke 1997; 28: 481–482.
- 36, , , . Absolute quantitation of diffusion constants in human stroke. Stroke 1997; 28: 483–490.
- 37, , , , , . Apparent diffusion coefficient mapping of experimental focal cerebral ischemia using diffusion-weighted echo-planar imaging. Magn. Reson. Med. 1993; 30: 318–325.Direct Link:
- 38, , . Cerebral white matter is highly vulnerable to ischemia. Stroke 1996; 27: 1641–1647.
- 39, , , , , . Different apparent diffusion coefficient: water content correlations of gray and white matter during early ischemia. Stroke 1998; 29: 859–865.
- 40, , , , , , , . Differences between gray mater and white matter water diffusion in stroke: diffusion-tensor MR imaging in 12 patients. Radiology 2000; 215: 211–220.
- 41, , , , , , , , , . Human acute cerebral ischemia: detection of changes in water diffusion anisotropy by using MR imaging. Radiology 1999; 212: 785–792.
- 42, , , , . A study of the apparent diffusion coefficient of grey and white matter in human stroke. NeuroReport 2000; 11: 2867–2874.
- 43, , , , , , . Reversal of DWI lesions may be associated with increases in anisotropy. Proc. Int. Soc. Magn. Reson. Med. 2000; 8: 778.
- 44, , , , . Diffusion anisotropy measurements in ischaemic stroke of the human brain. MAGMA 1998; 6: 28–36.
- 45, , , , , , , . Anisotropic water diffusion in white and gray matter of the neonatal piglet brain before and after transient hypoxia-ischemia. Magn. Reson. Imag. 1997; 15: 433–440.
- 46. Characterizing the target of acute stroke therapy. Stroke 1997; 28: 866–872.
- 47. Diffusion-weighted NMR imaging: application to experimental focal cerebral ischemia. NMR Biomed. 1995; 8: 345–358.Direct Link:
- 48, , , , . Investigation of techniques to quantify in vivo lesion volume based on comparison of ADCav maps with histology in focal cerebral ischemia studies of rats. Proc. Int. Soc. Magn. Reson. Med. 2000; 8: 474.
- 49
- 50, , , , , , . Reversal of acute apparent diffusion coefficient abnormalities and delayed neuronal death following transient focal brain ischemia in rats. Ann. Neurol. 1999; 46: 333–342.Direct Link:
- 51
- 52, , , . Temporal evolution of ischemic injury evaluated with diffusion-, perfusion-, and T2-weighted magnetic resonance imaging. Neurology 2000; 54: 689–696.
- 53, , , , , , . Transient and permanent resolution of ischemic lesions on diffusion-weighted imaging after brief periods of focal ischemia in rats: correlation with histopathology. Stroke 2000; 31: 946–954.
- 54, , , , , , , . Secondary decline in apparent diffusion coefficient and neurological after a short period of focal brain ischemia in rats. Ann. Neurol. 2000; 48: 236–244.Direct Link:
- 55, , , . Comparison of the temporal and spatial evolution of the water apparent diffusion coefficient and T2 following transient middle cerebral artery occlusion in rats. Proc. Int. Soc. Magn. Reson. Med. 2001; 9: 459.
- 56, , . Clinical outcome in ischemic stroke predicted by early diffusion-weighted and perfusion magnetic resonance imaging. J. Cereb. Blood Flow Metab. 1996; 16: 53–59.
- 57, , , , , , , . Determination of focal ischemic lesion volume in the rat brain using multispectral analysis. J. Magn. Reson. Imag. 1998; 8: 1266–1278.Direct Link:
- 58, , , , , , , , , , . Time course of ADCw changes in ischemic stroke: beyond the human eye! Stroke 1998; 29: 1778–1782.
- 59, , , , , , , . Unsupervised segmentation of multiparameter MRI in experimental cerebral ischemia with comparison to T2, diffusion, and ADC MRI parameters and histopathological validation. J. Magn. Reson. Imag. 2000; 11: 425–437.Direct Link:
- 60, , , , , , , . Histogram-based characterization of healthy and ischemic brain tissues using multiparametric MR imaging including apparent diffusion coefficient maps and relaxometry. Magn. Reson. Med. 2000; 43: 52–61.Direct Link:
- 61, , , , , , , , , , . Predicting tissue outcome in acute human cerebral ischemia using combined diffusion- and perfusion-weighted MR imaging. Stroke 2001; 32: 933–942.
- 62, , , , , , . A model for multiparametric MRI tissue characterization in experimental cerebral ischemia with histological validation in rat: part 1. Stroke 2001; 32: 943–949.
- 63, , , , , , , , . Multiparametric MRI tissue characterization in clinical stroke with correlation to clinical outcome: part 2. Stroke 2001; 32: 950–957.
- 64, , , , , , , , , . A strategy towards the automated estimation of stroke evolution utilising a diffusion and perfusion MRI based predictive model. Proc. Int. Soc. Magn. Reson. Med. 2001; 9: 314.
- 65, , , , , , , , , , . Spatial-temporal cluster analysis of serial diffusion tensor MRI in human cerebral ischemia. Proc. Int. Soc. Magn. Reson. Med. 2001; 9: 316.
- 66, , , , , . Topographical and quantitative assessment of white matter injury following a focal ischaemic lesion in the rat brain. Brain Res. Brain Res. Protoc. 1998; 2: 315–322.
- ADC
apparent diffusion coefficient
- ADCav
average apparent diffusion coefficient
- CSF
cerebrospinal fluid
- CBFi
cerebral blood flow index
- <D>
average diffusivity
- DTI
diffusion tensor imaging
- DWI
diffusion-weighted imaging
- FA
fractional anisotropy index
- GM
gray matter
- KM
k-means
- LI
lattice index anisotropy index
- mROI
mean normalized region of interest
- Mo
proton density
- MR
magnetic resonance
- ROI
region of interest
- SD
standard deviation
- SEM
standard error of the mean of the distribution
- T2
transverse relaxation time
- Tr(ADC)
trace of the diffusion tensor
- TTC
2, 3, 5-triphenyltetrazolium chloride
- WM
white matter
- μ
mean of the distribution
- λ1, λ2, λ3
eigenvalues of the diffusion tensor

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