Improvement of Pyramidal Tract Side Effect Prediction Using a Data-Driven Method in Subthalamic Stimulation

Objective: subthalamic nucleus deep brain stimulation (STN DBS) is limited by the occurrence of a pyramidal tract side effect (PTSE) induced by electrical activation of the pyramidal tract. Predictive models are needed to assist the surgeon during the electrode trajectory preplanning. The objective of the study was to compare two methods of PTSE prediction based on clinical assessment of PTSE induced by STN DBS in patients with Parkinson's disease. Methods: two clinicians assessed PTSE postoperatively in 20 patients implanted for at least three months in the STN. The resulting dataset of electroclinical tests was used to evaluate two methods of PTSE prediction. The first method was based on the volume of tissue activated (VTA) modeling and the second one was a data-driven-based method named Pyramidal tract side effect Model based on Artificial Neural network (PyMAN) developed in our laboratory. This method was based on the nonlinear correlation between the PTSE current threshold and the 3-D electrode coordinates. PTSE prediction from both methods was compared using Mann–Whitney U test. Results: 1696 electroclinical tests were used to design and compare the two methods. Sensitivity, specificity, positive- and negative-predictive values were significantly higher with the PyMAN method than with the VTA-based method (P < 0.05). Conclusion: the PyMAN method was more effective than the VTA-based method to predict PTSE. Significance: this data-driven tool could help the neurosurgeon in predicting adverse side effects induced by DBS during the electrode trajectory preplanning.

[1]  C. Honey,et al.  Electrophysiologic Validation of Diffusion Tensor Imaging Tractography during Deep Brain Stimulation Surgery , 2016, American Journal of Neuroradiology.

[2]  A. Lozano,et al.  Directional deep brain stimulation: an intraoperative double-blind pilot study. , 2014, Brain : a journal of neurology.

[3]  Pierre Jannin,et al.  Image-guided preoperative prediction of pyramidal tract side effect in deep brain stimulation: proof of concept and application to the pyramidal tract side effect induced by pallidal stimulation , 2016, Journal of medical imaging.

[4]  D. Louis Collins,et al.  Automated segmentation of basal ganglia and deep brain structures in MRI of Parkinson’s disease , 2012, International Journal of Computer Assisted Radiology and Surgery.

[5]  C. McIntyre,et al.  Current steering to control the volume of tissue activated during deep brain stimulation , 2008, Brain Stimulation.

[6]  A. Benabid Deep brain stimulation for Parkinson’s disease , 2003, Current Opinion in Neurobiology.

[7]  C. McIntyre,et al.  Artificial neural network based characterization of the volume of tissue activated during deep brain stimulation , 2013, Journal of neural engineering.

[8]  Caroline Essert,et al.  PyDBS: an automated image processing workflow for deep brain stimulation surgery , 2014, International Journal of Computer Assisted Radiology and Surgery.

[9]  Sébastien Ourselin,et al.  A three-dimensional, histological and deformable atlas of the human basal ganglia. I. Atlas construction based on immunohistochemical and MRI data , 2007, NeuroImage.

[10]  Matthew D. Johnson,et al.  Spatial steering of deep brain stimulation volumes using a novel lead design , 2011, Clinical Neurophysiology.

[11]  Alexandre Mendes,et al.  Intraoperative micro‐ and macrostimulation of the subthalamic nucleus in Parkinson's disease , 2002, Movement disorders : official journal of the Movement Disorder Society.

[12]  C. McIntyre,et al.  Role of electrode design on the volume of tissue activated during deep brain stimulation , 2006, Journal of neural engineering.

[13]  J. Volkmann,et al.  Basic algorithms for the programming of deep brain stimulation in Parkinson's disease , 2006, Movement disorders : official journal of the Movement Disorder Society.

[14]  Patrick van der Smagt,et al.  Introduction to neural networks , 1995, The Lancet.

[15]  Pierre Jannin,et al.  Analysis of electrode deformations in deep brain stimulation surgery , 2013, International Journal of Computer Assisted Radiology and Surgery.

[16]  James T. Patrie,et al.  Correlation of diffusion tensor tractography and intraoperative macrostimulation during deep brain stimulation for Parkinson disease. , 2014, Journal of neurosurgery.

[17]  Matthew D. Johnson,et al.  Current-controlled deep brain stimulation reduces in vivo voltage fluctuations observed during voltage-controlled stimulation , 2010, Clinical Neurophysiology.

[18]  C. Granziera,et al.  Sub-acute delayed failure of subthalamic DBS in Parkinson's disease: the role of micro-lesion effect. , 2008, Parkinsonism & related disorders.

[19]  Alistair Burns The benefits of early diagnosis of dementia , 2012, BMJ : British Medical Journal.

[20]  S. Cooper,et al.  Correlation Among Anatomic Landmarks, Location of Subthalamic Deep Brain Stimulation Electrodes, Stimulation Parameters, and Side Effects During Programming Monopolar Review , 2015, Neurosurgery.

[21]  C. McIntyre,et al.  Electric field and stimulating influence generated by deep brain stimulation of the subthalamic nucleus , 2004, Clinical Neurophysiology.

[22]  Abdelhamid Benazzouz,et al.  Imaging of subthalamic nucleus and ventralis intermedius of the thalamus , 2002, Movement disorders : official journal of the Movement Disorder Society.

[23]  J. Hughes,et al.  Accuracy of clinical diagnosis of idiopathic Parkinson's disease: a clinico-pathological study of 100 cases. , 1992, Journal of neurology, neurosurgery, and psychiatry.

[24]  J. Sim,et al.  The kappa statistic in reliability studies: use, interpretation, and sample size requirements. , 2005, Physical therapy.

[25]  W. Baxt Application of artificial neural networks to clinical medicine , 1995, The Lancet.

[26]  M. Vérin,et al.  Motor and non motor effects during intraoperative subthalamic stimulation for Parkinson’s disease , 2005, Journal of Neurology.

[27]  Jaimie M. Henderson,et al.  Patient-specific analysis of the volume of tissue activated during deep brain stimulation , 2007, NeuroImage.

[28]  Benoit M. Dawant,et al.  Effect of brain shift on the creation of functional atlases for deep brain stimulation surgery , 2010, International Journal of Computer Assisted Radiology and Surgery.

[29]  A. Benabid,et al.  Pyramidal tract side effects induced by deep brain stimulation of the subthalamic nucleus , 2007, Journal of Neurology, Neurosurgery, and Psychiatry.

[30]  C. McIntyre,et al.  Role of Soft-Tissue Heterogeneity in Computational Models of Deep Brain Stimulation , 2017, Brain Stimulation.

[31]  Hemant Bokil,et al.  Model-Based Deep Brain Stimulation Programming for Parkinson's Disease: The GUIDE Pilot Study , 2015, Stereotactic and Functional Neurosurgery.

[32]  Brian B. Avants,et al.  Symmetric diffeomorphic image registration with cross-correlation: Evaluating automated labeling of elderly and neurodegenerative brain , 2008, Medical Image Anal..

[33]  C. McIntyre,et al.  Cellular effects of deep brain stimulation: model-based analysis of activation and inhibition. , 2004, Journal of neurophysiology.

[34]  Nicholas Ayache,et al.  A three-dimensional histological atlas of the human basal ganglia. II. Atlas deformation strategy and evaluation in deep brain stimulation for Parkinson disease. , 2009, Journal of neurosurgery.

[35]  S. Adams,et al.  Clinical prediction rules , 2012, BMJ : British Medical Journal.

[36]  Michele Tagliati,et al.  Longitudinal Impedance Variability in Patients with Chronically Implanted DBS Devices , 2013, Brain Stimulation.