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      Evaluating Contextual Processing in Diffusion MRI: Application to Optic Radiation Reconstruction for Epilepsy Surgery

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          Abstract

          Diffusion MRI and tractography allow for investigation of the architectural configuration of white matter in vivo, offering new avenues for applications like presurgical planning. Despite the promising outlook, there are many pitfalls that complicate its use for (clinical) application. Amongst these are inaccuracies in the geometry of the diffusion profiles on which tractography is based, and poor alignment with neighboring profiles. Recently developed contextual processing techniques, including enhancement and well-posed geometric sharpening, have shown to result in sharper and better aligned diffusion profiles. However, the research that has been conducted up to now is mainly of theoretical nature, and so far these techniques have only been evaluated by visual inspection of the diffusion profiles. In this work, the method is evaluated in a clinically relevant application: the reconstruction of the optic radiation for epilepsy surgery. For this evaluation we have developed a framework in which we incorporate a novel scoring procedure for individual pathways. We demonstrate that, using enhancement and sharpening, the extraction of an anatomically plausible reconstruction of the optic radiation from a large amount of probabilistic pathways is greatly improved in three healthy controls, where currently used methods fail to do so. Furthermore, challenging reconstructions of the optic radiation in three epilepsy surgery candidates with extensive brain lesions demonstrate that it is beneficial to integrate these methods in surgical planning.

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          Most cited references 34

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          Robust determination of the fibre orientation distribution in diffusion MRI: non-negativity constrained super-resolved spherical deconvolution.

          Diffusion-weighted (DW) MR images contain information about the orientation of brain white matter fibres that potentially can be used to study human brain connectivity in vivo using tractography techniques. Currently, the diffusion tensor model is widely used to extract fibre directions from DW-MRI data, but fails in regions containing multiple fibre orientations. The spherical deconvolution technique has recently been proposed to address this limitation. It provides an estimate of the fibre orientation distribution (FOD) by assuming the DW signal measured from any fibre bundle is adequately described by a single response function. However, the deconvolution is ill-conditioned and susceptible to noise contamination. This tends to introduce artefactual negative regions in the FOD, which are clearly physically impossible. In this study, the introduction of a constraint on such negative regions is proposed to improve the conditioning of the spherical deconvolution. This approach is shown to provide FOD estimates that are robust to noise whilst preserving angular resolution. The approach also permits the use of super-resolution, whereby more FOD parameters are estimated than were actually measured, improving the angular resolution of the results. The method provides much better defined fibre orientation estimates, and allows orientations to be resolved that are separated by smaller angles than previously possible. This should allow tractography algorithms to be designed that are able to track reliably through crossing fibre regions.
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            The B-matrix must be rotated when correcting for subject motion in DTI data.

            To estimate diffusion tensor MRI (DTI) measures, such as fractional anisotropy and fiber orientation, reliably, a large number of diffusion-encoded images is needed, preferably cardiac gated to reduce pulsation artifacts. However, the concomitant longer acquisition times increase the chances of subject motion adversely affecting the estimation of these measures. While correcting for motion artifacts improves the accuracy of DTI, an often overlooked step in realigning the images is to reorient the B-matrix so that orientational information is correctly preserved. To the best of our knowledge, most research groups and software packages currently omit this reorientation step. Given the recent explosion of DTI applications including, for example, neurosurgical planning (in which errors can have drastic consequences), it is important to investigate the impact of neglecting to perform the B-matrix reorientation. In this work, a systematic study to investigate the effect of neglecting to reorient the B-matrix on DTI data during motion correction is presented. The consequences for diffusion fiber tractography are also discussed.
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              A randomized, controlled trial of surgery for temporal-lobe epilepsy.

              Randomized trials of surgery for epilepsy have not been conducted, because of the difficulties involved in designing and implementing feasible studies. The lack of data supporting the therapeutic usefulness of surgery precludes making strong recommendations for patients with epilepsy. We conducted a randomized, controlled trial to assess the efficacy and safety of surgery for temporal-lobe epilepsy. Eighty patients with temporal-lobe epilepsy were randomly assigned to surgery (40 patients) or treatment with antiepileptic drugs for one year (40 patients). Optimal medical therapy and primary outcomes were assessed by epileptologists who were unaware of the patients' treatment assignments. The primary outcome was freedom from seizures that impair awareness of self and surroundings. Secondary outcomes were the frequency and severity of seizures, the quality of life, disability, and death. At one year, the cumulative proportion of patients who were free of seizures impairing awareness was 58 percent in the surgical group and 8 percent in the medical group (P<0.001). The patients in the surgical group had fewer seizures impairing awareness and a significantly better quality of life (P<0.001 for both comparisons) than the patients in the medical group. Four patients (10 percent) had adverse effects of surgery. One patient in the medical group died. In temporal-lobe epilepsy, surgery is superior to prolonged medical therapy. Randomized trials of surgery for epilepsy are feasible and appear to yield precise estimates of treatment effects.
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                Author and article information

                Affiliations
                [1 ]Image Sciences Institute, University Medical Center Utrecht, Utrecht, The Netherlands
                [2 ]Department of Biomedical Engineering, Biomedical Image Analysis, Eindhoven University of Technology, Eindhoven, The Netherlands
                [3 ]Department of Mathematics and Computer Science, Eindhoven University of Technology, Eindhoven, The Netherlands
                [4 ]Department of Electrical Engineering, Mathematics and Computer Science, Delft University of Technology, Delft, The Netherlands
                [5 ]Department of Function and Medical Technology, Epilepsy Center Kempenhaeghe, Heeze, The Netherlands
                University of Minnesota, United States of America
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: PO RD AV PH LW CT. Performed the experiments: PO CT. Analyzed the data: PO PH LW CT. Contributed reagents/materials/analysis tools: RD AV BR PH LW AL PO CT. Wrote the paper: CT. Included patients: PO PH LW. Provided funding: RD AL. Critically reviewed manuscript: RD AV BR PH LW AL PO.

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, USA )
                1932-6203
                2014
                31 July 2014
                : 9
                : 7
                25077946 4117467 PONE-D-13-54780 10.1371/journal.pone.0101524

                This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                Counts
                Pages: 19
                Funding
                Chantal Tax is supported by a grant (No. 612.001.104) from the Physical Sciences division of the Netherlands Organisation for Scientific Research (NWO). The research leading to the results of this article has received funding from the European Research Council under the European Community's 7th Framework Programme (FP7/2007–2014)/ERC grant agreement No. 335555. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Anatomy
                Nervous System
                Neuroanatomy
                Neuroscience
                Neuroimaging
                Engineering and Technology
                Signal Processing
                Image Processing
                Medicine and Health Sciences
                Medical Physics
                Surgical and Invasive Medical Procedures
                Nervous System Procedures
                Neurosurgery
                Physical Sciences
                Mathematics
                Applied Mathematics
                Physics

                Uncategorized

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