|Year : 2003 | Volume
| Issue : 4 | Page : 433-440
|Diffusion weighted magnetic resonance imaging in acute ischemic stroke
C Kesavadas, M Fiorelli, AK Gupta, P Pantano, L Bozzao, TR Kapilamoorthy
Department of Radiology, Sree Chitra Tirunal Institute for Medical Sciences & Technology, Trivandrum-11, India
Click here for correspondence address and email
| Abstract|| |
Stroke is a leading cause of death and disability worldwide. With the advent of thrombolytic therapy in the treatment of acute stroke, it has become increasingly important to identify suitable patients for whom such therapy may be useful. Diffusion imaging has a high degree of sensitivity and specificity for diagnosing acute brain ischemia. The purpose of this article is to review the basis of diffusion weighted imaging (DWI), to consider its application in acute stroke and to recognize potential pitfalls and stroke mimics that might be encountered. Along with perfusion imaging. DWI helps in identifying the area of diffusion - perfusion mismatch representing the operational ischemic penumbra. Together with apparent diffusion coefficient (ADC) maps DWI images helps in distinguishing acute from subacute and chronic ischemic insults. The hyperintense area in DWI seen in acute brain ischemia can be reversed if early thrombolysis is instituted. In nearly half the patients with clinically defined transient ischaemic attack, DWI demonstrates ischaemic abnormality. The newer MR techniques developed for reducing susceptibility artifacts associated with diffusion imaging and the role of diffusion tensor imaging in the diagnosis of stroke have also been discussed in this review.
Keywords: Diffusion, Stroke, Ischemia, magnetic resonance imaging.
|How to cite this article:|
Kesavadas C, Fiorelli M, Gupta A K, Pantano P, Bozzao L, Kapilamoorthy T R. Diffusion weighted magnetic resonance imaging in acute ischemic stroke. Indian J Radiol Imaging 2003;13:433-40
Diffusion weighted imaging (D I) has now become a routine technique in the magnetic resonance (MR) protocols for the evaluation of stroke patients. In 1986, the intravoxel incoherent motion and diffusion Imaging was introduced by Le Bihan ,. However only by the mid 1990s the method became a routine in clinical practice because of its demanding MR engineering requirements especially high performance magnetic field gradients. Its primary application has been in the investigation of acute stroke patients where it provides a unique information about the physiologic state of ischemic tissue. It also helps in distinguishing irreversible ischemic lesions from potentially reversible lesion characterized by vasogenic oedema.
|How to cite this URL:|
Kesavadas C, Fiorelli M, Gupta A K, Pantano P, Bozzao L, Kapilamoorthy T R. Diffusion weighted magnetic resonance imaging in acute ischemic stroke. Indian J Radiol Imaging [serial online] 2003 [cited 2019 Nov 16];13:433-40. Available from: http://www.ijri.org/text.asp?2003/13/4/433/28729
| Biophysical basis|| |
Diffusion is referred to as random microscopic motion of water molecules. Diffusion depends on several factors including the type of particle or molecule under study, the temperature and the environment in which it takes place. The tissue water diffusion is lower than free water diffusion because of restriction due to fibers, membranes and macromolecules. The diffusion coefficient means the diffusivity of a particle or molecule in a certain medium. Any pathophysiological process (such as cerebral ischemia) which modifies the integrity of the cell membranes and myelin fibers can result in a change in the diffusion coefficient. With MR imaging, the molecular motion caused by concentration gradients cannot be differentiated from molecular motion caused by pressure gradients, thermal gradients or ionic interactions. Therefore when measuring molecular motion with DWI, the rate of molecular motion is influenced by several factors and only the apparent diffusion coefficient (ADC) (not the true diffusion coefficient) can be measured.
The possibility of measuring the diffusion coefficient using MR techniques was first put forward by Stejskal and Tanner in 1963 . The relationship between signal intensity (S) of a voxel and the rate of apparent diffusion can be expressed as
S = So x exp (-b x ADC)
Where So is the signal intensity of the T2 weighted image. The degree of diffusion weighting expressed by the b value can be adjusted by the strength and time between the rising edges of the diffusing sensitizing gradient.
b = r2GS2 ( ∆ - S/3)
where r is the gyro magnetic ratio, G is the magnitude of, S is the width of, and ∆ is the time between the two balanced gradients. By repeating the experiment with varying b value the ADC can be determined.
The ADC is not the same in all directions (not isotropic) in the brain. The apparent diffusion varies in different directions (anisotropic) primarily because of the underlying anatomic structure of the tissue. . The anisotropic nature of diffusion can be appreciated by comparing images obtained with diffusion gradients applied in 3 different orthogonal directions.
Diffusion gradient is applied in one direction at a time. The three images obtained by applying diffusion gradient in 3 different directions are multiplied. The cube root of the product is the DW image. The DW image has T2 contrast and contrast due to ADC difference. To remove the T2 contrast, the DW image can be divided by the T2 image (b=0) to get the so called exponential image. Alternatively an ADC map in which the signal intensity corresponds to the magnitude of ADC can be created.
| Technique|| |
DWI is usually done by using a single shot echoplanar imaging (EPI) spin echo T2 weighted sequence with the diffusion encoding paired gradient pulses applied in 3 orthogonal directions and with the b value at 0 and 1000 s/mm2. This ultrafast imaging approach tends to minimize gross motion artifact. However it brings with it intrinsic sensitivity to magnetic field inhomogenity (magnetic susceptibility artifact). This artifact increases with increasing magnetic strength. Parallel imaging strategies such as SENSE  allows dramatic shortening of EPI read out train reducing the blurring. The absolute TE can be reduced for the same diffusion sensitivity, leading to reduced magnetic susceptibility - related artifact allowing visualization of anatomic territories difficult for good visualization by echo planar imaging technique.
Another successful approach to reduce susceptibility artifact is to acquire images with a novel k- space sampling technique known as PROPELLER . Although this fast spin echo based technique takes longer imaging time it has utility in obtaining high quality DW MR images at the skull base and other areas prone to artifact.
The major non-diffusion effect contributing to hyperintensity in DWI is the T2 shine through effect. This effect is due to contamination of DW images by T2 signal hyper intensity resulting from lesions with T2 prolongation. The ADC map or the exponential image can be utilized for estimating the age of the ischemic lesion since both these images are not influenced by T2 contamination.
As an alternative to these post processing strategies pulse sequence developers seek to obtain similar diffusion sensitivities at even shorter TE (to decrease T2 effects) by using stronger diffusion encoding gradients. Similarly for a given T2 weighting, attempts are being made to increase the b-value so that the contribution from diffusion process is emphasized.
| Evolution of diffusion changes in cerebral ischemia|| |
Moseley and others were the first to observe hyperintensity in the ischemic territory within minutes of vascular occlusion when DWI was done in animal models ,. The signal contrast between the ischemic and the normal side is so much that it was called the "the light bulb sign for acute stroke". This compares with the subtle early sign in non-contrast CT (eg. Insular ribbon sign, loss of grey /white matter differentiation, hyperdense MCA) .
Cerebral ischemia below a critical cerebral blood flow threshold results in disruption of energy metabolism with consequent failure of ion pumps and anoxic cell membrane depolarization. The activity of the ion pumps (NaK ATPase pump) is ATP dependent. As local cerebral blood flow drops below a critical threshold the energy supply to such cells becomes inadequate and the activity of this pump fails and the cells begin to swell. The membrane permeability is increased and water shifts from the extracellular space to the intacellular space resulting in cytotoxic edema ,. Decrease in the apparent diffusion coefficient (ADC) of the ischemic brain tissue has been shown to coincide with the onset of this cytotoxic edema  and this area is seen as area of hyperintensity in the DWI  and hypointensity in ADC images [Figure - 1],[Figure - 2].
Over time as the ischemic cascade progresses, cells ;lyse and the macrophage activity increases leading to an evolution towards vasogenic edema, observable more in the T2 weighted images. In this period of transition from acute to sub-acute and chronic stroke, there are significant changes in the temporal evolution of diffusion changes. Following reduction in the acute phase the ADC values re-normalize several days (approx 7-10 days) after stroke onset and then increase in the ensuing days and weeks , [Figure - 3]. Thus a knowledge of the time of onset of clinical symptoms with the timing of DWI is critical for appropriate interpretation (see [Table - 1]). As an advantage of this series of phenomenon DWI and ADC maps can be used to distinguish acute from sub acute ischemic insults of the brain.
The time course pattern described earlier is not always followed. Early reperfusion may cause renormalization of the reduced ADC at a much earlier time point as early as 1 to 2 days in human who received recombinant tissue plasminogen activator (rtPA) administered within 3 hours of stroke onset .
| Reliability of DWI in acute stroke|| |
New thrombolytic and neuro protective therapies are being developed to treat acute ischemic infarction. Good results have been shown if the treatment is undertaken within the first 3 hours ,. Hence early detection of the ischemic region has gained a lot of importance in recent years. After a stroke, detection of hypoattenuation in CT scan and hyperintensity on T2 weighted images require a substantial increase in tissue water. For infarction imaged within 6 hours of stroke onset, reported sensitivities are 38% to 45% for CT scan and 18% to 46% for MR imaging ,. Diffusion weighted imaging has shown to be highly sensitive (88-100%) and specific (86%-100%) in the detection of hyperacute and acute infarction ,,,. A large series of 691 patients presenting to the emergency department has shown that DWI is superior to MR imaging, first and second CT in the examination of patients with acute stroke within 24 hours of presentation. The superiority is most clearly demonstrated when the imaging is performed in less than or equal to 6 hours following presentation . After 24 hours DWI and ADC maps helps in distinguishing between acute, sub acute and chronic lesions. This is of great help especially in older patients who have T2 hype rintensities that may be indistinguishable from acute lesions in T2 and FLAIR images.
False negative DWI lesions has been reported for lacunar brain stem or deep grey matter infarcts  and in regions of decreased perfusion in perfusion MR imaging. Many of these lesions are picked up in the follow up DWI. False positive DWI lesions with restricted diffusion can be seen in cerebral abscess (due to high viscosity) and in tumor (due to dense cellularity). Differentiation can be made by viewing routine T1, T2 weighted and post contrast images.
DWI can help in differentiation of stroke sub-types (Lacunar vs Embolic) which may be necessary in deciding the patient management. Lacunar strokes remain a relative contraindication to thrombolytic therapy because of their spontaneous potential for complete recovery and risk of intracranial hemorrhage with rt-PA use. Clinical differentiation of large vessel from small vessel strokes may be inaccurate. One out of 6 cases that appear to be classic lacunar syndrome on clinical evaluation has multiple infarctions, probably due to embolic cause, demonstrated on DWI . Hence, the use of DWI to uncover subsidiary infarctions in patients with lacunar syndromes should prompt the physicians to search for an underlying embolic source and tailor a secondary stroke prevention strategy to treat the underlying cause.
| Diffusion - Perfusion Mismatch|| |
Perfusion imaging involves detection of decrease in signal resulting from the T2 susceptibility effects of gadolinium during the passage of bolus of gadolinium through the intracranial vasculature. This decrease in signal will be low in setting of an area of reduced perfusion . Various haemodynamic images are created which include regional cerebral blood volume (rCBV), regional cerebral blood flow (rCBF), mean transit time (MTT), and time to peak (TTP) maps.
With early stroke there is frequently a region characterized by normal diffusion but abnormal perfusion (diffusion - perfusion mismatch) that is thought to represent the operational ischemic penumbra . The penumbra is characterized by tissue that is ischemic but still viable and may infarct if not treated. Proximal occlusions are far more likely to result in mismatch than distal or lacunar infarction. The brain regions with decreased diffusion and decreased perfusion are believed to represent non-viable tissue or the core of an infarction . A diffusion lesion larger than the perfusion lesion or diffusion lesion without a perfusion abnormality usually occurs with early reperfusion. In such situation the diffusion lesions will not change significantly overtime.
Efforts are underway to identify specific MR signatures and criteria to identify regions of reversible vs. irreversible infarction . Though several studies have tried to analyze the various diffusion and perfusion indices, a recent study showed that rCBF ratio is the most useful parameter in distinguishing hypoperfused tissue that progressed to infarction from hypoperfused tissue that remained viable in the ischemic penumbra . Further characterisation of the MR signatures of penumbra and core infarction may allow extension of the time window for treatment beyond current standards, basing treatment decisions on individual patient pathophysiology rather than rigid time windows.
DWI along with perfusion imaging has also been helpful in defining the mechanism of the borderzone infarction, I Transient perfusion deficits occurring with hypotension in the absence of a critical large-artery disease is usually accompanied by a normal PWI. Embolism may cause small perfusion deficits in the borderzone territory matching the area of diffusion abnormality. Critical large- I artery occlusive disease is usually associated with large territorial perfusion deficits and predisposes to borderzone infarction .
Another study has shown the usefulness of DWI and perfusion imaging in determining reperfusion after thrombolytic therapy. After successful reperfusion, the final perfusion deficits are less than or equal to the initial DWI hyperintensity and correlate with functional outcome.
| Reversibility|| |
Although the area identified as hyperintense in DWI is often labeled as infarct this may not be true. This area may show evidence of energy failure and cell regulation defect, however, the cells might not have progressed to ultimate death. Hence there is a definite role to salvage even this so called "infarcted area".
In humans in the absence of thrombolysis reversibility of DWI lesion is rare. In a review of DWI reversible lesions, Karonen et al could identify only 21 of thousands of DWI hyperintense lesions that demonstrated reversibility . In animal models a threshold time of around 2 hours has been established for reversibility  and a resolution or decrease of the size of the diffusion lesion has been shown if the occlusion in the artery is released within this time.
In the setting of intravenous and intra-arterial thrombolysis a decrease in lesion size from the initial DWI abnormality to the final infarct size or a partial reversibility of the initial DWI is common ,. At this point it has to be highlighted that acute reperfusion induced normalization of ADC values appear to be a poor predictor of ultimate tissue recovery, since secondary irreversible damage may develop . Hence cases in which DWI or ADC maps appear normal in the sub acute phase must be judged with caution.
| Transient Ischemic Attacks (TIA)|| |
DWI demonstrates ischemic abnormalities in nearly half of clinically defined TIA patients . The lesions are usually less than 15mm in maximal diameter. The percentage of patients with positive DWI lesion increases with increasing total symptom duration . The compromised vascular territory detected on diffusion imaging and the clinical symptoms correlate. In nearly half the patients the diffusion MRI changes may be fully reversible, while in the remainder the findings herald the development of a parenchymal infarct despite transient ,clinical symptoms. Ay et al suggested an increased j stroke risk in patients with these lesions . Kidwell et al showed that in one third of TIA patients the DWI result had significant clinical utility by changing the presumed localization and etiologic mechanism of the ischemic lesion .
| Correlation of DWI with Clinical outcome|| |
It has been seen in earlier studies that a combination of DWI images with NIHSS (National Institute of Health Stroke scale score) may predict clinical recovery of cortical infarcts than any of the factors taken alone . Statistically significant correlation has been found between the acute diffusion MR lesion volume and both acute and chronic neurological assessment tests ,. Patients with perfusion deficits larger than the diffusion MR lesion volume had worse clinical outcome  compared to those patients who had early reperfusion .
| Diffusion tensor imaging (DTI)|| |
DWI is inherently one dimensional technique, i.e. it is used to measure the projection of all molecular displacements long one direction at a time. Therefore it is sufficient to apply the diffusion gradients along only one direction. DTI is inherently three dimensional; one must apply diffusion gradients in at least six non collinear, non-coplanar directions in order to provide enough information to estimate the six independent elements of the diffusion tensor equation . In an anisotropic medium like white matter [Figure - 4] where the measured diffusivity is known to depend upon orientation of the tissue, no single ADC can charecterise the orientation dependent water mobility in these tissues. Moreover the ability of DTI to distinguish between the relatively isotropic grey matter and anisotrpic white matter allows separate quantitative assessment of the response of these tissues to ischemic injury . The differences in neuronal structure between white matter and grey matter make it likely that the mechanism of ischemic injury and strategies of protection will vary  DTI may thus allow separate evaluation of treatment response of white matter and grey matter to neuroprotective therapy. The measurement of diffusion anisotropy may provide means of evaluating cerebral ischemia in a time independent fashion .
| Cytotoxic versus Vasogenic Edema|| |
Diffusion MR imaging can reliably distinguish vasogenic from cytotoxic edema. Vasogenic edema is characterized by elevated diffusion caused by a relative increase in water in the extracellular compartment where the water is mobile and cytotoxic edema is characterized by restricted diffusion. Vasogenic edema is hypointense to slightly hyperintense in DWI. When hyperintense it can mimic hyperacute to subacute infarction and hence ADC maps should be looked into to differentiate from cytotoxic edema. On ADC images cytotoxic edema caused by ischemia is always hypointense for 1 to 2 weeks and vasogenic edema is hyperintense. Differentiating these two entities affects patient management and outcome.
Syndromes with reversible vasogenic edema include ecclampsia, hypertensive encephalopathy, cyclosporin toxicity and other posterior leukoencephalopathies, venous thrombosis HIV encephalopathy and hyperperfusion syndrome following carotid endarterectomy. Patients with these syndromes can present with neurological deficits raising the suspicion of acute ischemic stroke
| Entities with Restricted Diffusion in DWI|| |
There are few conditions characterized by restricted diffusion on DWI images (hyperintensity in DWI and hypointensity in ADC images) which can be mistaken for acute ischemic stroke. The clinical picture in each of these conditions is usually different from stroke.
Infection : Abscess cavities and empyemas have restricted diffusion due to high viscosity and cellularity of pus . Gadolinium enhanced imaged will help to distinguish this condition from acute stroke. Herpes encephalitis can have an area of cytotoxic edema. However usually it does not respect any vascular territory, rather it involves the temporal lobes. Creutzfeldt Jacob disease have also demonstrated lesions characterized by low ADCs in the cortex and basal ganglia .
Diffuse Axonal Injury: In humans, diffuse axonal injury may be characterized by restricted diffusion as long as 18 days after injury .
Demyelinative lesions : Acute MS plaques rarely may show restricted diffusion due to cytotoxic oedema and increased inflammatory cellular infiltration  These plaques may demonstrate a ring enhancing pattern which may help to differentiate from acute infarction.
Epilepsy : DWI can show hyperintensity in the cerebral cortex and a decrease in ADC on the side of epileptic focus .
Mass lesions : Restricted diffusion can be seen in highly cellular tumors likely lymphoma.
Hemorrhage : Oxy haemoglobin is characterized by restricted diffusion and is hyperintense to normal brain tissue on DWI. This may be due to relative restriction of water movement inside the red blood cell. Hence there is a likelihood of mistaking it with acute stroke. However CT will be able to differentiate both since the hemorrhage will look hyperdense.
Hemorrhagic transformation : is a potentially dangerous complication after acute ischemic stroke. A method for identifying patients at increased risk for developing secondary hemorrhagic transformation (HT) could be of significant value, particularly in patients being considered for thrombolytic therapy. Recent studies suggest that DW I can help predict the risk of intracerebral hemorrhage after thrombolysis . HT-destined stroke regions possess a significantly great percentage of low ADC values than non-HT-destined regions. Thus early measurement of ADC values may be a useful tool for assessing secondary HT risk .
In summary diffusion MR imaging is a highly sensitive and specific technique in the detection of acute and hyperacute ischemic stroke has greatly improved the diagnosis and treatment of acute stroke.
| Acknowledgement|| |
The authors would like to thank the Ministry of Foreign Affairs, Govt. of Italy and the department of Science & Technology, Govt. Of India for funding the Indo-Italian scientific collaboration project (MH6).
The authors also thank the Department of Neurological Sciences, University of Rome, for giving permission to do the studies and write the articles.
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Department of Neurological Sciences, Universita di Roma "La Sapienza" Viale dell' Universita, 30 00185 Roma
Source of Support: None, Conflict of Interest: None
[Figure - 1], [Figure - 2], [Figure - 3], [Figure - 4]
[Table - 1]
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