MR Diffusion Imaging in Ischemic Stroke

doi:10.1016/j.nic.2011.03.001

Neuroimaging Clinics of North America

Volume 21, Issue 2, May 2011, Pages 345-377

https://doi.org/10.1016/j.nic.2011.03.001 Get rights and content

Section snippets

Basic concepts of diffusion MR imaging

The term, diffusion, refers to the general transport of matter whereby molecules or ions mix through normal agitation in a random way. When describing the mixing of different liquids or gases, diffusion is described in terms of a concentration gradient of the diffusing substance. In biologic tissues, the driving force is the motion of water within water, driven by thermal agitation and commonly referred to as Brownian motion. For example, the path of a pollen grain suspended in water provides

Basic mechanisms underlying restricted diffusion associated with acute stroke

Much of the understanding of the mechanisms underlying DWI changes in acute ischemic stroke is based on experimental animal models of cerebral ischemia. Cerebral ischemia results in decreased diffusion of water molecules within the infarct territory with a rapid decline in ADC values that can be attributed to a combination of complex biophysical factors resulting from disruption of normal cellular metabolism with depletion of ATP (Box 1). These processes result in failure of Na⁺/K⁺ ATPase and

Diffusion-weighted imaging map interpretation

All DWIs (linearly T2-weighted and exponentially diffusion-weighted) should be reviewed with ADC maps (linearly diffusion-weighted, without a T2 component) and/or exponential images (exponentially diffusion-weighted, without a T2 component) (Fig. 4). The use of the ADC map and/or exponential image is essential for proper interpretation of DWIs because both areas of diminished and increased diffusion can appear bright on DWIs. In acute ischemic lesions with restricted diffusion, the T2 and

Time course of DWI changes associated with acute ischemia

After the onset of acute ischemia, there is a rapid decrease in water diffusion that is markedly hyperintense on DWI and hypointense on the ADC map (Fig. 7, 6 and 9 hours; Table 1). After the initial ADC decrease, there is a gradual increase in the ADC values secondary to cell lysis and increasing vasogenic edema, with a return to baseline known as pseudonormalization, when the ADC of the nonviable ischemic tissue is similar to normal brain ADC (see Fig. 7, 5 days). In stroke animal models, ADC

Reliability and pitfalls of DWI in identification of acute ischemic lesions

DWI is highly sensitive (81–100%) and specific (86–100%) for detection of acute ischemia within the first 12 hours after stroke symptom onset,23, 24, 25, 26, 27 with sensitivities and specificities in the 90–100% range at specialized stroke centers (Box 2). DWI can demonstrate acute ischemic lesions as early as 11 minutes after symptom onset.²⁸ DWI is superior to conventional MR imaging and CT in the first 6 hours because there is usually insufficient increase in tissue water for reliable

Reversibility of DWI-positive lesions in ischemic stroke and use of DWI for determination of infarct core

It is widely accepted that DWI is the best method for identifying infarct core or tissue destined to progress to infarction (see Box 2). In the absence of early reperfusion in the setting of IV thrombolytic therapy or IA recanalization procedures, reversibility of decreased diffusion (DWI abnormality on the initial scan without a corresponding abnormality on follow-up FLAIR or T2-weighted MR images) is rare. Frequently, the final infarct volume includes the initial area of diffusion abnormality

Use of DWI for predicting hemorrhagic transformation

HT of brain infarcts represents bleeding into ischemic tissue that usually occurs some time after the initial insult (Fig. 14). The reported incidence of HT varies widely, in part due to differences in definitions, imaging examinations (CT vs MR imaging with or without gradient-echo images), and timing of follow-up imaging. The incidence is clearly increased, however, after thrombolytic therapy and ranges from 6% up to 44% if susceptibility sensitive MR imaging sequences are used. The incidence

Correlation of DWI lesion volume with clinical outcome

Initial DWI and ADC lesion volumes correlate with clinical outcome measured by various acute and chronic neurologic assessment tests, including the National Institutes of Health Stroke Scale, the Glasgow Outcome Scale, the Barthel Index and the Rankin Scale or Modified Rankin Scale (see Box 2).19, 45, 46, 77, 78, 79, 80 Reported correlations range from r = 0.56 to r = 0.73. Because many of the commonly used clinical scoring systems are weighted toward motor symptoms and language, usually

Diffusion tensor imaging and diffusion kurtosis imaging

Although DWI has been useful in the clinical management of stroke, DTI (Table 3) and DKI (Table 4) may offer additional diagnostic information on the microstructural status of tissue because there is directional dependence of diffusion in tissue known as anisotropy. Diffusion in tissue is affected by the presence of semipermeable membranes and oriented structures in the intracellular, extracellular, and vascular compartments that result in preferential movement of water parallel to them. In the

The diffusion tensor

Anisotropy can be characterized by the effective diffusion tensor D, a second-order tensor with 9 components describing molecular mobility along each direction and correlation between these directions⁸⁵: $D = [\begin{matrix} D_{x x} & D_{x y} & D_{x z} \\ D_{y x} & D_{y y} & D_{y z} \\ D_{z x} & D_{z y} & D_{z z} \end{matrix}]$ The components of D can be estimated by noting the effect of anisotropic diffusion on the MR imaging signal is given by⁸⁶ $S = S_{0} \exp (- \sum_{i = x, y, z} \sum_{j = x, y, z} b_{i j} D_{i j})$ where b_ij are components in the b matrix, which is equivalent to the b-value used to characterize

The diffusion kurtosis tensor

In conventional DTI analysis, the probabilistic distribution of water diffusion is assumed to be Gaussian with the standard deviation along each eigenvector direction proportional to the corresponding diffusion coefficient forming a diffusion ellipsoid. Biologic tissues, however, are inherently heterogeneous, with multiple compartments formed by semipermeable membranes and oriented microstructures in the intracellular, extracellular, and vascular domains, which result in non-Gaussian

DTI and DKI in the normal brain

Visual inspection of MD and average ADC maps of the normal adult brain generally shows no significant image contrast between gray matter and white matter, consistent with studies demonstrating relatively uniform average diffusion throughout the developed adult brain.⁹³ In contrast, white matter tracts are highly anisotropic and easily discriminated from relatively isotropic gray matter on RA, FA, VR, and lattice index maps.93, 100 This is supported by increased diffusional heterogeneity in

Evolution of mean diffusion in ischemia

Serial longitudinal DTI studies after ischemic stroke demonstrate time course values for MD derived from trace of D that are similar to those of ADC.127, 128, 129, 130 One advantage of DTI over conventional DWI is the ability to segment white matter from gray matter based on their differences in anisotropy. No significant difference in MD is observed between gray matter and white matter in hyperacute stroke,131, 132 but several studies have shown a 5% to 20% greater decrease in MD of ischemic

Evolution of diffusional anisotropy in ischemia

Diffusional anisotropy varies widely throughout the brain, including different white matter regions, due to differences in underlying microstructural architecture.⁹³ Therefore, any alteration in diffusional anisotropy within a particular brain region is always reported relative to the corresponding region in the normal contralateral hemisphere.

In both rats¹³⁷ and monkeys,¹³⁸ a mild increase in FA up to 20% is observed within minutes after MCA occlusion. FA remains elevated for up to 2 hours in

Diffusional kurtosis changes in ischemia

Only a few studies have used DKI and related q-space imaging to follow changes in non-Gaussian behavior of water diffusion in human cerebral ischemia. Similar to diffusion anisotropy, diffusional kurtosis varies widely throughout the brain, including different white matter regions, due to differences in underlying microstructural architecture.109, 112 Evolution of DKI parameter changes in ischemic stroke is summarized in Table 1.

Peeters and colleagues,¹⁴³ in a study using q-space imaging to

Predicting tissue viability and clinical outcome

At present, the role of DTI in assessing hyperacute stroke is still uncertain. Although DTI has longer acquisition and postprocessing times than DWI, using a single-shot EPI technique with an efficient diffusion gradient-encoding scheme,¹⁵³ the full diffusion tensor can be obtained within minutes.131, 132 FA elevation in hyperacute infarction is at most 20% relative to contralateral normal tissue,131, 132 and the difference is borderline significant at best. Relative changes in other diffusion

Secondary white matter degeneration

Secondary degeneration of white matter tracts remote from the primary ischemic region can be classified into antegrade (Wallerian) degeneration toward the axonal terminal and retrograde degeneration toward the neuronal body. Histologically, it is characterized by disintegration of axonal structures, myelin degradation, infiltration by macrophages, and gliosis.¹⁷¹

DTI has been used to assess Wallerian degeneration of the CST in patients with hemiparesis172, 173, 174 and to distinguish Wallerian

Perinatal hypoxic-ischemic injury

MR imaging, including DTI, is becoming the imaging modality of choice for assessing hypoxic-ischemic injury in neonates because of its sensitivity in detecting brain injury and the association of MR imaging findings with neurodevelopmental outcome. The time course of MD in regions of brain injury from perinatal hypoxic-ischemic events in term neonates has been described by several investigators.183, 184, 185, 186 Although MD is decreased in most neonates within 24 hours after injury, the amount

Summary

Diffusion MR imaging has vastly improved evaluation of acute ischemic stroke. It is highly sensitive and specific in the detection of acute ischemic stroke at early time points when CT and conventional MR imaging sequences are unreliable. The initial DWI lesion is thought to represent infarct core and usually progresses to infarction unless there is early reperfusion. The initial DWI lesion volume correlates highly with final infarct volume as well as with acute and chronic neurologic

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Cited by (82)

Intravoxel incoherent motion and diffusion kurtosis imaging at 3T MRI: Application to ischemic stroke
2023, Magnetic Resonance Imaging
The DKI-IVIM model that incorporates DKI (diffusional kurtosis imaging) into the IVIM (Intravoxel Incoherent Motion) concept was investigated to assess its utility for both enhanced diffusion characterization and perfusion measurements in ischemic stroke at 3 T.
Fifteen stroke patients (71 ± 11 years old) were enrolled and DKI-IVIM analysis was performed using 9 b-values from 0 to 1500 s/mm² chosen with the Cramer-Rao-Lower-Bound optimization approach. Pseudo-diffusion coefficient D*, perfusion fraction f, blood flow-related parameter fD*, the diffusion coefficient D and an additional parameter, the kurtosis, K were determined in the ischemic lesion and controlateral normal tissue based on a region of interest approach. The apparent diffusion coefficient (ADC) and arterial spin labelling (ASL) cerebral blood flow (CBF) parameters were also assessed and parametric maps were obtained for all parameters.
Significant differences were observed for all diffusion parameters with a significant decrease for D (p < 0.0001), ADC (p < 0.0001), and a significant increase for K (p < 0.0001) in the ischemic lesions of all patients. f decreased significantly in these regions (p = 0.0002). The fD* increase was not significant (p = 0.56). The same significant differences were found with a motion correction except for fD* (p = 0.47). CBF significantly decreased in the lesions. ADC was significantly positively correlated with D (p < 0.0001) and negatively with K (p = 0.0002); K was also negatively significantly correlated with D (p = 0.01).
DKI-IVIM model enables for simultaneous cerebral perfusion and enhanced diffusion characterization in an acceptable clinically acquisition time for the ischemic stroke diagnosis with the additional kurtosis factor estimation, that may better reflect the microstructure heterogeneity.
Reduced diffusion in white matter after radiotherapy with photons and protons
2021, Radiotherapy and Oncology
Radio(chemo)therapy is standard in the adjuvant treatment of glioblastoma. Inevitably, brain tissue surrounding the target volume is also irradiated, potentially causing acute and late side-effects. Diffusion imaging has been shown to be a sensitive method to detect early changes in the cerebral white matter (WM) after radiation. The aim of this work was to assess possible changes in the mean diffusivity (MD) of WM after radio(chemo)therapy using Diffusion-weighted imaging (DWI) and to compare these effects between patients treated with proton and photon irradiation.
70 patients with glioblastoma underwent adjuvant radio(chemo)therapy with protons (n = 20) or photons (n = 50) at the University Hospital Dresden. MRI follow-ups were performed at three-monthly intervals and in this study were evaluated until 33 months after the end of therapy. Relative white matter MD changes between baseline and all follow-up visits were calculated in different dose regions.
We observed a significant decrease of MD (p < 0.05) in WM regions receiving more than 20 Gy. MD reduction was progressive with dose and time after radio(chemo)therapy (maximum: −7.9 ± 1.2% after 24 months, ≥50 Gy). In patients treated with photons, significant reductions of MD in the entire WM (p < 0.05) were seen at all time points. Conversely, in proton patients, whole brain MD did not change significantly.
Irradiation leads to measurable MD reduction in white matter, progressing with both increasing dose and time. Treatment with protons reduces this effect most likely due to a lower total dose in the surrounding white matter. Further investigations are needed to assess whether those MD changes correlate with known radiation induced side-effects.
On the potential for mapping apparent neural soma density via a clinically viable diffusion MRI protocol
2021, NeuroImage
Diffusion MRI is a valuable tool for probing tissue microstructure in the brain noninvasively. Today, model-based techniques are widely available and used for white matter characterisation where their development is relatively mature. Conversely, tissue modelling in grey matter is more challenging, and no generally accepted models exist. With advances in measurement technology and modelling efforts, a clinically viable technique that reveals salient features of grey matter microstructure, such as the density of quasi-spherical cell bodies and quasi-cylindrical cell projections, is an exciting prospect. As a step towards capturing the microscopic architecture of grey matter in clinically feasible settings, this work uses a biophysical model that is designed to disentangle the diffusion signatures of spherical and cylindrical structures in the presence of orientation heterogeneity, and takes advantage of B-tensor encoding measurements, which provide additional sensitivity compared to standard single diffusion encoding sequences. For the fast and robust estimation of microstructural parameters, we leverage recent advances in machine learning and replace conventional fitting techniques with an artificial neural network that fits complex biophysical models within seconds. Our results demonstrate apparent markers of spherical and cylindrical geometries in healthy human subjects, and in particular an increased volume fraction of spherical compartments in grey matter compared to white matter. We evaluate the extent to which spherical and cylindrical geometries may be interpreted as correlates of neural soma and neural projections, respectively, and quantify parameter estimation errors in the presence of various departures from the modelling assumptions. While further work is necessary to translate the ideas presented in this work to the clinic, we suggest that biomarkers focussing on quasi-spherical cellular geometries may be valuable for the enhanced assessment of neurodevelopmental disorders and neurodegenerative diseases.
Novel proton exchange rate MRI presents unique contrast in brains of ischemic stroke patients
2020, Journal of Neuroscience Methods
To map and quantify the proton exchange rate ( $k_{e x}$ ) of brain tissues using improved omega plots in ischemic stroke patients and to investigate whether $k_{e x}$ can serve as a potential endogenous surrogate imaging biomarker for detecting the metabolic state and the pathologic changes due to ischemic stroke.
Three sets of Z-spectra were acquired from seventeen ischemic stroke patients using a spin echo-echo planar imaging sequence with pre-saturation chemical exchange saturation transfer (CEST) pulse at $B_{1}$ of 1.5, 2.5, and 3.5 $μ T$ , respectively. Pixel-wise $k_{e x}$ was calculated from improved omega plot of water direct saturation (DS)-removed Z-spectral signals.
The derived $k_{e x}$ maps can differentiate infarcts from contralateral normal brain tissues with significantly increased signal (893 ± 52 $s^{- 1}$ vs. 739 ± 34 $s^{- 1}$ , P < 0.001).
The $k_{e x}$ maps were found to be different from conventional contrasts from diffusion-weighted imaging (DWI), CEST, and semi-solid magnetization transfer (MT) MRI. In brief, $k_{e x}$ MRI showed larger lesion areas than DWI with different degrees and different lesion contrast compared to CEST and MT.
In this preliminary translational research, the $k_{e x}$ MRI based on DS-removed omega plots has been demonstrated for in vivo imaging of clinical ischemic stroke patients. As a noninvasive and unique MRI contrast, $k_{e x}$ MRI at 3 T may serve as a potential surrogate imaging biomarker for the metabolic changes of stroke and help for monitoring the evolution and the treatment of stroke.
Reduced diffusion in normal appearing white matter of glioma patients following radio(chemo)therapy
2019, Radiotherapy and Oncology
Citation Excerpt :
Additionally, it has been shown that demyelinated white matter in mice shows significantly increased T2* [29], whereas we observe a significant T2* decrease. The MD reduction in white matter following radiotherapy is mainly driven by a reduction in RD. A decrease in RD in white matter is usually associated with axonal swelling, as observed in acute and early phases of stroke [30]. However, in our study the RD decrease was in the order of 10%, compared to well over 50% in stroke and therefore not easily assessed visually.
Standard treatment of high grade gliomas includes gross tumour resection followed by radio(chemo)therapy. Radiotherapy inevitably leads to irradiation of normal brain tissue. The goal of this prospective, longitudinal study was to use MRI to quantify normal appearing white and grey matter changes following radiation treatment as a function of dose and time after radiotherapy.
Pre-radiotherapy (proton or photon therapy) MRI and follow-up MRIs collected in 3 monthly intervals thereafter were analysed for 22 glioma patients and included diffusion tensor imaging, quantitative T1, T2* and proton density mapping. Abnormal tissue was excluded from analysis. MR signal changes were quantified within different dose bin regions for grey and white matter and subsequently for whole brain white matter.
We found significant reductions in mean diffusivity, radial diffusivity, axial diffusivity and T2* in normal appearing white matter regions receiving a radiation dose as low as 10–20 Gy within the observational period of up to 18 months. The magnitude of these changes increased with the received radiation dose and progressed with time after radiotherapy. Whole brain white matter also showed a significant reduction in radial diffusivity as a function of radiation dose and time after radiotherapy. No significant changes were observed in grey matter.
Diffusion tensor imaging and T2* imaging revealed normal appearing white matter changes following radiation treatment. The changes were dose dependant and progressed over time. Further work is needed to understand the underlying tissue changes and to correlate the observed diffusion changes with late brain malfunctions.
A study of neurite orientation dispersion and density imaging in ischemic stroke
2019, Magnetic Resonance Imaging
Citation Excerpt :
An increased ODI in lesions in this study may reflect the real pathological changes during ischemic stroke. Because axons and dendrites swell and bead, the loss of myelin sheath and the breaking of WM fibers led to the increased complexity of neurite orientation dispersion [2,20,23]. Viso represents the diffusion fraction with the isotropic Gaussian property, which was very small compared with Vic and ODI values in normal brain tissues and was found to be reduced in the lesion regions.
To demonstrate the feasibility of the neurite orientation dispersion and density imaging (NODDI) technique in characterizing the microstructural changes in brain tissues during ischemic stroke and to compare its sensitivity with diffusion tensor imaging (DTI) and diffusion kurtosis imaging (DKI).
Seventy-one patients with hyperacute/acute/subacute ischemic stroke were enrolled in the study. A multishell diffusion magnetic resonance imaging (dMRI) protocol was performed for each subject. Diffusion data were analyzed using the NODDI and diffusional kurtosis estimator toolboxes. Then, NODDI metrics between the lesions and the contralateral tissues were compared to evaluate their values in ischemic stroke. NODDI metrics among different stroke periods and the correlations between NODDI and the duration since stroke onset were analyzed as well. To compare the NODDI's sensitivity with established diffusion techniques, paired t-tests were performed to determine the absolute percentage changes of diffusion metrics between NODDI and DTI/DKI.
Compared with the contralateral tissues, lesions showed significantly increased values of intracellular volume fraction (V_ic) and orientation dispersion index (ODI) and decreased values of isotropic volume fraction (V_iso). ODI value was significantly different among three periods and showed fair to good positive correlation with the duration since stroke onset (R = 0.450). NODDI metrics showed significantly larger absolute percentage changes than that of DTI and DKI (P < 0.05, respectively).
NODDI allowed efficient evaluation of microstructural changes in brain tissues during ischemic stroke and showed increased sensitivity compared with DTI and DKI. The possible biophysical mechanisms underlying ischemia could be further elucidated using this advanced diffusion technique.

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MR Diffusion Imaging in Ischemic Stroke

Section snippets

Basic concepts of diffusion MR imaging

Basic mechanisms underlying restricted diffusion associated with acute stroke

Diffusion-weighted imaging map interpretation

Time course of DWI changes associated with acute ischemia

Reliability and pitfalls of DWI in identification of acute ischemic lesions

Reversibility of DWI-positive lesions in ischemic stroke and use of DWI for determination of infarct core

Use of DWI for predicting hemorrhagic transformation

Correlation of DWI lesion volume with clinical outcome

Diffusion tensor imaging and diffusion kurtosis imaging

The diffusion tensor

The diffusion kurtosis tensor

DTI and DKI in the normal brain

Evolution of mean diffusion in ischemia

Evolution of diffusional anisotropy in ischemia

Diffusional kurtosis changes in ischemia

Predicting tissue viability and clinical outcome

Secondary white matter degeneration

Perinatal hypoxic-ischemic injury

Summary

First page preview

Biophys J

Lancet

Eur J Radiol

Eur J Radiol

J Neurol Sci

J Magn Reson

J Magn Reson

J Magn Reson

J Magn Reson

J Magn Reson B

Sodium ion apparent diffusion coefficient in living rat brain

Magn Reson Med

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

Mechanism of detection of acute cerebral ischemia in rats by diffusion-weighted magnetic resonance microscopy

Stroke

In vivo excitotoxicity induced by ouabain, a Na+/K+-ATPase inhibitor

J Cereb Blood Flow Metab

Cytotoxic brain edema: assessment with diffusion-weighted MR imaging

Radiology

Evaluation of extra- and intracellular apparent diffusion in normal and globally ischemic rat brain via 19F NMR

Magn Reson Med

Evaluation of extra- and intracellular apparent diffusion coefficient of sodium in rat skeletal muscle: effects of prolonged ischemia

Magn Reson Med

Transient hypoxia-ischemia in rats: changes in diffusion-sensitive MR imaging findings, extracellular space, and Na+-K+ -adenosine triphosphatase and cytochrome oxidase activity

Radiology

Effects of osmotically driven cell volume changes on diffusion-weighted imaging of the rat optic nerve

Magn Reson Med

Dynamic changes in water ADC, energy metabolism, extracellular space volume, and tortuosity in neonatal rat brain during global ischemia

Magn Reson Med

Diffusion of metabolites in normal and ischemic rat brain measured by localized 1H MRS

Magn Reson Med

Evaluation of intracellular diffusion in normal and globally-ischemic rat brain via 133Cs NMR

Magn Reson Med

Theoretical model for water diffusion in tissues

Magn Reson Med

A model to predict the histopathology of human stroke using diffusion and T2-weighted magnetic resonance imaging

Stroke

Magnetic resonance imaging assessment of evolving focal cerebral ischemia. Comparison with histopathology in rats

Stroke

Time course of the apparent diffusion coefficient (ADC) abnormality in human stroke

Neurology

Fast magnetic resonance diffusion-weighted imaging of acute human stroke

Neurology

Time course of lesion development in patients with acute stroke: serial diffusion- and hemodynamic-weighted magnetic resonance imaging

Stroke

Serial analysis of the apparent diffusion coefficient time course in human stroke

Neuroradiology

Acute human stroke studied by whole brain echo planar diffusion-weighted magnetic resonance imaging

Ann Neurol

Ischemic stroke: effects of etiology and patient age on the time course of the core apparent diffusion coefficient

Radiology

Diffusion-weighted MR imaging: diagnostic accuracy in patients imaged within 6 hours of stroke symptom onset

Radiology

Sensitivity and interrater agreement of CT and diffusion-weighted MR imaging in hyperacute stroke

AJNR Am J Neuroradiol

Detectability and detection rate of acute cerebral hemisphere infarcts on CT and diffusion-weighted MRI

Neuroradiology