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British Journal of Radiology 74 (2001),642-647 © 2001 The British Institute of Radiology

Short communication

MR diffusion tensor imaging of white matter tract disruption in stroke at 3 T

J H Gillard, BSc, MD, FRCR 1, N G Papadakis, PhD 2,5 K Martin 5 C J S Price, BSc, MRCP 3 E A Warburton, MA, DM, MRCP 3 N M Antoun, FRCP, FRCR 1 C L-H Huang, PhD 2 T A Carpenter, PhD 5 and J D Pickard, MA, MChir, FRCS 4,5

Departments of 1Radiology, 2Physiology, 3Neurology and 4Neurosurgery and 5The Wolfson Brain Imaging Centre, University of Cambridge, Cambridge CB2 2QQ, UK


   Abstract
Top
 Abstract
Introduction
 Methods and patients
 Results
 Discussion
 Conclusion
 References
 
Recent advances in MR diffusion weighted imaging (DWI) enable the identification of anisotropic white matter tracts with diffusion tensor imaging (DTI). We aimed to use a novel DTI technique to safely study patients with recent stroke in a high field (3 T) MR machine with its intrinsically higher spatial resolution and signal-to-noise ratio. Of ten patients studied, six had disruption of white matter tracts as determined by DTI. A further patient had distortion of white matter tracts around an infarct rather than actual disruption of the tracts themselves. The lack of tract destruction may imply a beneficial prognosis, information that is not available with conventional DWI.


   Introduction
Top
 Abstract
 Introduction
Methods and patients
 Results
 Discussion
 Conclusion
 References
 
Recent advances in MR methodologies now enable rapid identification of ischaemic tissue in acute stroke. Techniques such as diffusion weighted imaging (DWI) [1–3] appear to delineate infarcted tissue [4–6]. Abnormalities demonstrated using MR perfusion imaging [7] and MR spectroscopic imaging [8] potentially identify areas at risk of infarction in the ischaemic penumbra. The challenges in imaging of very early stroke are centred on the identification of potentially salvageable tissue and the assessment of whether there is a major vascular occlusion or not, the aim being to give appropriate targeted therapy to identifiable subtypes of stroke. A less well addressed problem relates to the use of imaging to provide prognostic information regarding clinical outcome.

DWI and the extracted apparent diffusion coefficient (ADC) maps examine diffusion only along a defined spatial direction. Biological tissues possess varying degrees of structural organization at the macromolecular, membrane and cellular levels. Their diffusion properties, therefore, are typically anisotropic [9–11] and consequently can only be fully characterized through the symmetric 3 x 3 diffusion tensor, which comprises six independent scalar elements at the macroscopic scale of an imaging voxel [12]. Diffusion tensor imaging (DTI) has recently been proposed [12] and implemented for the in vivo study of cerebral [13] and cardiac [14] disease, enabling complete directional descriptions to be made of the self-diffusion properties of water through the tissue structure.

The ability to identify white matter tract disruption in acute stroke may be a useful index of stroke severity and may allow insight into likely recovery and long-term disability. There have been limited studies using DTI at conventional MR field strengths (1.5 T) in subacute stroke. The advent of very high strength magnetic fields (=>3 T), with their increased spatial resolution and signal-to-noise ratio, potentially allows for clearer identification of white matter disruption. The aim of this preliminary study was to use a novel high field DTI technique in the assessment of patients with stroke in an environment that allows the safe monitoring of acutely unwell patients whilst they are being imaged.


   Methods and patients
Top
 Abstract
 Introduction
 Methods and patients
Results
 Discussion
 Conclusion
 References
 
Ten patients presenting with stroke were imaged. Their demographics are presented in Table 1Go. Experiments were performed on a 3 T whole body system consisting of a Bruker Medspec 30/100 spectrometer (Bruker Medical, Etlingen, Germany) attached to an Oxford 3.0 T, 910 mm bore whole body actively shielded magnet (Oxford Magnet Technology, Oxford, UK). The whole body gradient coil had an internal diameter of 63 cm (Bruker, BG630), was actively shielded and had a maximum strength per axis of 35 mT m-1, using 225 µs ramps. DTI was performed using a standard single shot, spin echo, echo planar imaging (EPI) pulse sequence, inserting a pair of diffusion weighted (DW) Stejskal–Tanner rectangular gradient pulses in it [15]. The duration {Delta} of the DW gradient pulses was 21 ms and their temporal spacing {delta} was 66 ms. The DTI protocol consisted of 63 acquisitions in total. The DW gradients were applied along 12 non-collinear spatial directions uniformly arranged [16]. For each direction, five DW images were acquired, each corresponding to a different b value [15]. These five b values were distributed equidistantly in the interval (0–1570) s mm-2, with 1570 s mm-2 corresponding to optimum noise performance for a 2-point ADC measurement [16, 17]. The adverse effects of eddy currents on single shot DW EPI [18] were efficiently eliminated by a robust adjustment of the pre-emphasis unit of the system, as described by Papadakis et al [19]. Multislice imaging was performed with 8–12 contiguous slices in the near axial plane, with 5 mm slice thickness and 25 cm field of view. The acquisition matrix was 128 x 128 and sampling dwell time was 5 µs. Asymmetric k-space coverage was performed along the phase encode direction (24% of the data acquired prior to reaching the centre of k-space). The echo time (TE) was 106 ms and the repetition time (TR) was 5070 ms. No other intermediate processing step, such as image realignment or correction (due to eddy current induced distortions), was required owing to the efficient elimination of eddy current induced distortions achieved by the robust pre-emphasis adjustment [19]. Subsequently, maps of the rotationally invariant isotropy index (mean value of the trace Tr(D) of the diffusion tensor D and the rotationally invariant anisotropy index relative anisotropy (RA) [13, 20]) were calculated.


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  		Table 1. Patient demographic data

 
Patients underwent a full clinical examination prior to the MR study. The diffusion tensor images were reviewed both as soft and hard copy, as were the conventional T2 and proton density weighted images. Specific reference was made to whether there was white matter tract disruption or distortion.

Ethical approval was obtained from the Local Research Ethics Committee of Addenbrooke's Hospital. Informed consent was obtained from each subject.


   Results
Top
 Abstract
 Introduction
 Methods and patients
 Results
Discussion
 Conclusion
 References
 
DTI was successfully performed in nine patients, one study being a technical failure due to patient movement artefact. No patient died during the study period. DTI took approximately 5 min; total post-processing time was approximately 15 min. All patients demonstrated DWI changes acquired with b=1000 s mm-2. DTI was initially abnormal in seven patients. The abnormalities consisted of actual disruption of white matter tracts in six patients. Patient No. 3 demonstrated initial displacement of white matter tracts rather than tract breakdown (Figure 1Go), which was associated with good clinical outcome at 4 months. Patient No. 9, imaged 11 h from stroke onset, had no tract disruption at presentation, with only subtle changes in the DWI study. The study was repeated 6 days later when the DWI abnormality was more extensive and there was definite disruption of white matter tracts (Figure 2Go). No patient demonstrated white matter tract changes distant to the acute stroke.



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  		Figure 1. Two representative slices from the diffusion tensor images (A,B) and the trace images (C,D) in a 55-year-old male smoker (patient No. 3) who presented with a right hemiplegia, right seventh nerve palsy and dysarthria. The diffusion tensor imaging demonstrates displacement of the internal and external capsules (arrows) by an acute stroke based on the left corpus striatum extending into the corona radiata. The trace images confirm an acute ischaemic event.

 


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  		Figure 2. A 25-year-old smoker (patient No. 9) presented with dysphasia and a right hemiparesis. Diffusion tensor images (A,B) are normal. The initial trace images (C,D) demonstrate a subtle area of increased signal in the anterior left putamen. The patient was re-imaged at 6 days, which demonstrated disruption of white matter tracts in the left corona radiata (E) with associated trace map changes (F) confirming early ischaemia.

 

   Discussion
Top
 Abstract
 Introduction
 Methods and patients
 Results
 Discussion
Conclusion
 References
 
This study has demonstrated that it is feasible to image acutely unwell stroke patients at 3 T, and that the diffusion tensor images can be obtained quickly and are able to delineate disruption in white matter tracts with good spatial resolution without artefact from cerebral spinal fluid pulsation. Furthermore, the ability to demonstrate distortion of tracts as well as partial or complete disruption may enable the technique to provide an indicator of likely functional deficit or recovery. As the sequence did not allow whole brain coverage, we may have missed distal effects such as cerebellar diaschisis.

DWI has been shown to be an effective tool in the diagnosis of tumours [21], demyelination [22], head injury [23] and stroke [4–6] even though these methods only examine diffusion along a defined direction. Measurement of the self-diffusion tensor D on a pixel-by-pixel basis can also lead to the calculation of scalar quantities, known as indices of anisotropy [24]; they reflect the degree of anisotropy of water diffusion and hence are related to the degree of architectural and structural coherence of the tissue within each pixel. Since a loss of tissue order and organization often occurs in abnormal development, aging and degeneration, such quantities are of significant clinical value not only for tissue structural and functional [25] studies but also in conditions such as stroke [26], traumatic brain injury [27], schizophrenia [28] and Wallerian degeneration [29]. Most studies to date have been at a field strength of 1.5 T.

A number of optimizations were performed to refine the DTI sequence, which included appropriate positioning of the DW gradient pulses with maximum temporal separation (for a given TE) that resulted in efficient diffusion weighting. Asymmetric k-space coverage along the phase encode direction reduced the TE. It was found that the asymmetry used (24%) was optimum (further asymmetry would lead to image artefacts) and thus T2, T2* effects were minimized. Diffusion tensor sampling was optimized using 12 uniformly arranged DW directions [16].

Such sampling significantly increases the accuracy and precision of DTI compared with schemes using the standard 6–7 DW directions. The maximum b value (bmax) used corresponded to the optimum noise performance for a 2-point ADC measurement, with the ADC equal to the mean value of the trace for normal brain parenchyma (D=0.7 x 10-3 mm2 s-1) [16, 17]. The optimum noise performance for a 2-point ADC measurement was therefore used as an objective criterion for selection of bmax. Finally, since the protocol entailed five signal acquisitions per DW direction, there were two alternatives: (i) to have all these acquisitions at the same b value, bmax (signal averaging); or (ii) to have them at different b values equally spaced between 0 and bmax. We used the second approach because it leads to better estimation of the anisotropic diffusion tensor compared with the first approach [16].

Mismatch between MR perfusion and DWI provides insight into tissue at risk of infarction that might benefit from therapeutic interventions. The techniques have been used in the assessment of patients receiving thrombolysis for acute ischaemic stroke [30]. DTI may provide an additional indicator of stroke pathophysiology, possibly allowing further differentiation of different stroke subtypes that may require differing therapeutic strategies. Sorensen et al [31] have recently shown significant changes in anisotropy in white matter in patients undergoing acute stroke. They noted much smaller changes in grey matter, a finding that has been corroborated by Mukherjee et al [26]. Whilst we found DTI changes most marked within white matter, the complementary trace images provided important information concerning grey matter ischaemia, allowing for an integrated assessment. Normative DTI data are now becoming available [32]. The DTI study of patient No. 3 showed distortion of the internal and external capsules secondary to ischaemia in the putamen. Tract distortion from adjacent oedematous tissue is not unexpected, however we feel that the lack of tract destruction may imply a beneficial prognosis, information that is not available with conventional DWI.


   Conclusion
Top
 Abstract
 Introduction
 Methods and patients
 Results
 Discussion
 Conclusion
References
 
We have shown that it is possible to safely perform DTI at high field strength in patients with acute stroke. The technique has the ability to identify white matter tract disruption as well as distortion, which may prove to be useful in the diagnostic and therapeutic management of acute stroke.


   Acknowledgments
 
The help of Tim Donovan is greatly appreciated.


   Footnotes
 
Technology Foresight, Medical Research Council, funded this study. Back

Received for publication October 18, 2000. Revision received February 22, 2001. Accepted for publication April 4, 2001.


   References
Top
 Abstract
 Introduction
 Methods and patients
 Results
 Discussion
 Conclusion
 References
 

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