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Assessment of a method to determine deep brain stimulation targets using deterministic tractography in a navigation system

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Abstract

Recent advances in imaging permit radiologic identification of target structures for deep brain stimulation (DBS) for movement disorders. However, these methods cannot detect the internal subdivision and thus cannot determine the appropriate DBS target located within those subdivisions. The aim of this study is to provide a straightforward method to obtain an optimized target (OT) within DBS target nuclei using a widely available navigation system. We used T1- and T2-weighted images, fluid-attenuated inversion recovery (FLAIR) sequence, and diffusion tensor imaging (DTI) of nine patients operated for DBS in our center. Using the StealthViz® software, we segmented the targeted deep structures (subcortical targets) and the anatomically identifiable areas to which these target nuclei were connected (projection areas). We generated fiber tracts from the projection areas. By identifying their intersections with the subcortical targets, we obtained an OT within the DBS target nuclei. We computed the distances from the clinically effective electrode contacts (CEEC) to the OT obtained by our method and the targets provided by the atlas. These distances were compared using a Wilcoxon signed-rank test, with p < 0.05 considered statistically significant. We were able to identify OT coincident with the motor part of the subthalamic nucleus and the ventral intermediate nucleus. We clinically tested the results and found that the CEEC were significantly more closely related to the OT than with the targets obtained by the atlas. Our present results show that this novel method permits optimization of the stimulation site within the internal subdivisions of target nuclei for DBS.

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Acknowledgments

This work was supported by Instituto de Salud Carlos III, grant number PI10/1932. The authors thank Dr. Juan Alvarez-Linera for the image acquisition, Juan Sobrado and Julio Gonzalez for the technical support in the software, and Mrs. Ingrid Carranza for the support and assistance in the figures, tables, and illustrations.

Disclosures

The authors have no personal financial or institutional interest in any of the materials or devices described in this article.

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Comments

Tetsuya Goto, Matsumoto, Japan

The authors reported the useful target measuring method in deep brain stimulation surgery guided by MRI tractography. Their methodology looks reasonable and agreeable. They concluded that their advocating target was superior to using atlas-based target (x −12 mm, y −3 mm, z −4 mm from AC-PC line) because it was nearer to the most clinically effective electrode contact point than atlas-based target.

When the stereotactic surgery guided by microrecording is performed, the initial target should be determined by not only the final target point in the dorsolateral STN but also the insertion point, trajectory angle, ventricle size, and thickness of thalamus. The most clinically effective electrode contact point is not also the initial target because it is decided after checking the effectiveness of treatment and the complications of side effects. The authors moved the target two or three times, although they were guided by their method. The selection of the initial target might be discussed by the number of times of the trajectory.

If the direct visualization of the STN is possible by using their method, it may be superior to conventional technique. These techniques will shift the paradigm from the microrecording-guided to radiographic-guided stereotactic surgery. They will reduce the number of times of the trajectory, risk of hemorrhage, and operation time.

Peter Grunert, Homburg/Saar, Germany

An intrinsic problem in functional stereotaxy is the fact that in most of the cases, the target is not directly visible in the images neither in ventriculography nor in CT or in MRI. Therefore, indirect methods based on a human atlas have been developed to determine the target point in relation to defined anatomical landmarks such as the anterior and posterior commissure. Additionally, intraoperative microelectrode recording and electric stimulation were routinely intraoperatively applied during deep brain stimulation to optimize the target for the final placement of the electrode. The authors in this contribution proposed a new method for optimizing the target point by visualization of the afferent or efferent tracts to or from the target area. For the STN, they visualized the connections of this nucleus to the cortical motor and several premotor areas. For the VIM nucleus in the thalamus, they were able to demonstrate the efferent fibers from dentate and ruber nucleus to the area of the VIM. This was achieved in MRI images by the meanwhile established method of fiber tracking. Despite several technical limitations of this method, the authors could show that their optimized target calculation based on tractography was statically more close to the final target established by electrophysiological methods than the calculation based on a stereotactic atlas.

I think this is a very interesting and original contribution with great potential in the future. The tractography with the visualization of the well-known anatomical afferent and efferent connections seems to be a very logical and promising method to optimize the target even within the target area. In the future, with better image resolution, tractography may make the time-consuming electrophysiological testing superfluous. However, at this point of development, in particular for small target areas, the electrophysiological investigations are still indispensible.

Jürgen Voges, Magdeburg, Germany

This manuscript describes a procedure using deterministic tractography (DTI) to improve stereotactic targeting. The integration of DTI into stereotactic treatment planning protocols for DBS surgery seems logical because it is widely accepted that large fibers originating in or projecting onto the stimulated area play a prominent role in mediating the beneficial effects of neurostimulation. Referred to the here examined targets, crucial fiber tracts are the “hyperdirect pathway” in the case of the subthalamic nucleus or the “dentatorubrothalamic tract” (DRT) when the ventral intermediate thalamic nucleus is electrically stimulated. If direct targeting of fiber tracts instead of relais nuclei will improve the clinical outcome is not yet clearly defined. Schlaier and collaborators, for instance, addressing intraoperative tremor improvement as a function of the spatial relationship of active electrode contacts and the DRT, reported that the distance to this fiber tract had no impact on the outcome (1). The findings of Coenen et al., in contrast, displayed a trend for better tremor response when active electrode contacts projected onto the DRT in comparison to those contacts located at the anterior border of this tract, but this difference was statistically not significant (2).

General concerns, when using clinical tractography, refer to the anatomic accuracy of this method. Thomas and colleagues investigated in-depth the assumption that the combination of high-resolution diffusion-weighted imaging and sophisticated diffusion modeling approaches may provide anatomically correct connectivity maps of the brain. Comparing the “visualized” connections with those derived from tracer studies—the “gold standard”—this group demonstrated that suboptimal information accuracy results from inherent methodological limitations of tractography. According to their conclusions, comprehensive methodological modifications are required to overcome these limitations (3). Related to stereotactic treatment planning, tractography cannot replace electrophysiology and/or intraoperative clinical testing at that time, and keeping the aforementioned methodological problems in reference, it is recommended to use DTI skeptically.

References

1. Schlaier J, Anthofer J, Steib K, Fellner C, Rothenfusser E, Brawanski A, Lange M. Deep brain stimulation for essential tremor: targeting the dentato-rubro-thalamic tract? Neuromodulation 2014.

2. Coenen VA, Allert N, Paus S, Kronenburger M, Urbach H, Madler B. Modulation of the cerebello-thalamo-cortical network in thalamic deep brain stimulation for tremor: a diffusion tensor imaging study. Neurosurgery 2014;75:657–670.

3. Thomas C, Ye FQ, Irfanoglu MO, Modi P, Saleem KS, Leopold DA, Pierpaoli C. Anatomical accuracy of brain connections derived from diffusion MRI tractography is inherently limited. Proc Natl Acad Sci U S A 2014;111:16574–16579.

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Avecillas-Chasin, J.M., Alonso-Frech, F., Parras, O. et al. Assessment of a method to determine deep brain stimulation targets using deterministic tractography in a navigation system. Neurosurg Rev 38, 739–751 (2015). https://doi.org/10.1007/s10143-015-0643-1

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