The subthalamic nucleus at 7.0 Tesla: evaluation of sequence and orientation for deep-brain stimulation

BackgroundDeep-brain stimulation (DBS) of the subthalamic nucleus (STN) is an accepted neurosurgical technique for the treatment of medication-resistant Parkinson’s disease and other neurological disorders. The accurate targeting of the STN is facilitated by precise and reliable identification in pre-stereotactic magnetic resonance imaging (MRI).The aim of the study was to compare and evaluate different promising MRI methods at 7.0 T for the pre-stereotactic visualisation of the STNMethodsMRI (T2-turbo spin-echo [TSE], T1-gradient echo [GRE], fast low-angle shot [FLASH] two-dimensional [2D] T2* and susceptibility-weighted imaging [SWI]) was performed in nine healthy volunteers. Delineation and image quality for the STN were independently evaluated by two neuroradiologists using a six-point grading system. Inter-rater reliability, contrast-to-noise ratios (CNRs) and signal-to-noise ratios (SNRs) for the STN were calculated. For the anatomical validation, the coronal FLASH 2D T2* images were co-registered with a stereotactic atlas (Schaltenbrand-Wahren).ResultsThe STN was clearly and reliably visualised in FLASH 2D T2* imaging (particularly coronal view), with a sharp delineation between the STN, the substantia nigra and the zona incerta. No major artefacts in the STN were observed in any of the sequences. FLASH 2D T2* and SWI images offered significantly higher CNR for the STN compared with T2-TSE. The co-registration of the coronal FLASH 2D T2* images with the stereotactic atlas affirmed the correct localisation of the STN in all cases.ConclusionThe STN is best and reliably visualised in FLASH 2D T2* imaging (particularly coronal orientation) at 7.0-T MRI.

[1]  Jaimie M Henderson,et al.  Clinical Motor Outcome of Bilateral Subthalamic Nucleus Deep-Brain Stimulation for Parkinson's Disease Using Image-Guided Frameless Stereotaxy , 2010, Neurosurgery.

[2]  S. Schoenberg,et al.  Gadofosveset: Parameter Optimization for Steady-State Imaging of the Thoracic and Abdominal Vasculature , 2011, Investigative radiology.

[3]  Jens Volkmann,et al.  Bilateral high-frequency stimulation in the subthalamic nucleus for the treatment of Parkinson disease: correlation of therapeutic effect with anatomical electrode position. , 2002, Journal of neurosurgery.

[4]  Y. Wu,et al.  Determination of brain iron content in patients with Parkinson’s disease using magnetic susceptibility imaging , 2009, Neuroscience bulletin.

[5]  Angelo Antonini,et al.  Parkinson's disease tremor-related metabolic network: Characterization, progression, and treatment effects , 2011, NeuroImage.

[6]  C. McIntyre,et al.  Uncovering the mechanism(s) of action of deep brain stimulation: activation, inhibition, or both , 2004, Clinical Neurophysiology.

[7]  Y. Agid,et al.  Stimulation of subterritories of the subthalamic nucleus reveals its role in the integration of the emotional and motor aspects of behavior , 2007, Proceedings of the National Academy of Sciences.

[8]  A L Benabid,et al.  Treatment of tremor in Parkinson's disease by subthalamic nucleus stimulation , 1998, Movement disorders : official journal of the Movement Disorder Society.

[9]  Y. Agid,et al.  Bilateral subthalamic stimulation for Parkinson's disease by using three-dimensional stereotactic magnetic resonance imaging and electrophysiological guidance. , 2000, Journal of neurosurgery.

[10]  Didier Dormont,et al.  Is the subthalamic nucleus hypointense on T2-weighted images? A correlation study using MR imaging and stereotactic atlas data. , 2004, AJNR. American journal of neuroradiology.

[11]  A L Benabid,et al.  Deep brain stimulation of the subthalamic nucleus for Parkinson's disease: methodologic aspects and clinical criteria. , 2000, Neurology.

[12]  K. Uğurbil,et al.  An Assessment of Current Brain Targets for Deep Brain Stimulation Surgery With Susceptibility-Weighted Imaging at 7 Tesla , 2010, Neurosurgery.

[13]  S. Paek,et al.  Bilateral Subthalamic Deep Brain Stimulation in Parkinson Disease Patients With Severe Tremor , 2010, Neurosurgery.

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

[15]  Murray Grossman,et al.  Deep brain stimulation in neurologic disorders. , 2007, Parkinsonism & related disorders.

[16]  J. Hogg Magnetic resonance imaging. , 1994, Journal of the Royal Naval Medical Service.

[17]  R A Bakay,et al.  Magnetic resonance imaging-based stereotactic localization of the globus pallidus and subthalamic nucleus. , 1999, Neurosurgery.

[18]  D. Roberts,et al.  Magnetic resonance imaging versus computed tomography for target localization in functional stereotactic neurosurgery. , 1999, Neurosurgery.

[19]  D. Sakas,et al.  Neurosurgery for psychiatric disorders: from the excision of brain tissue to the chronic electrical stimulation of neural networks. , 2007, Acta neurochirurgica. Supplement.

[20]  P D Griffiths,et al.  Iron in the basal ganglia in Parkinson's disease. An in vitro study using extended X-ray absorption fine structure and cryo-electron microscopy. , 1999, Brain : a journal of neurology.

[21]  Yu-Chung N. Cheng,et al.  Susceptibility weighted imaging (SWI) , 2004, Zeitschrift fur medizinische Physik.

[22]  Val M Runge,et al.  Brain Tumor Enhancement in Magnetic Resonance Imaging: Comparison of Signal-to-Noise Ratio (SNR) and Contrast-to-Noise Ratio (CNR) at 1.5 Versus 3 Tesla , 2005, Investigative radiology.

[23]  Jean-Pierre Lin,et al.  Childhood disorders of neurodegeneration with brain iron accumulation (NBIA) , 2011, Developmental medicine and child neurology.

[24]  A. Lozano,et al.  Direct visualization of deep brain stimulation targets in Parkinson disease with the use of 7-tesla magnetic resonance imaging. , 2010, Journal of neurosurgery.

[25]  Hoon-Ki Min,et al.  Evolution of Deep Brain Stimulation: Human Electrometer and Smart Devices Supporting the Next Generation of Therapy , 2009, Neuromodulation : journal of the International Neuromodulation Society.

[26]  Val M Runge,et al.  Simulation and assessment of cerebrovascular damage in deep brain stimulation using a stereotactic atlas of vasculature and structure derived from multiple 3- and 7-tesla scans. , 2010, Journal of neurosurgery.

[27]  Paul Krack,et al.  Electrophysiological mapping for the implantation of deep brain stimulators for Parkinson's disease and tremor , 2006, Movement disorders : official journal of the Movement Disorder Society.

[28]  J. Duyn,et al.  Magnetic susceptibility mapping of brain tissue in vivo using MRI phase data , 2009, Magnetic resonance in medicine.

[29]  D. Bowers,et al.  Do patient's get angrier following STN, GPi, and thalamic deep brain stimulation , 2011, NeuroImage.

[30]  P. Limousin,et al.  The Physiological Effects of Pallidal Deep Brain Stimulation in Dystonia , 2007, IEEE Transactions on Neural Systems and Rehabilitation Engineering.

[31]  Shabbar F. Danish,et al.  Brain Shift during Deep Brain Stimulation Surgery for Parkinson’s Disease , 2007, Stereotactic and Functional Neurosurgery.

[32]  Richard S. Frackowiak,et al.  Confirmation of functional zones within the human subthalamic nucleus: Patterns of connectivity and sub-parcellation using diffusion weighted imaging , 2012, NeuroImage.

[33]  S. Ellias,et al.  Assessment of the variability in the anatomical position and size of the subthalamic nucleus among patients with advanced Parkinson’s disease using magnetic resonance imaging , 2010, Acta Neurochirurgica.

[34]  Tarek A. Yousry,et al.  A Quick and Universal Method for Stereotactic Visualization of the Subthalamic Nucleus before and after Implantation of Deep Brain Stimulation Electrodes , 2004, Stereotactic and Functional Neurosurgery.

[35]  A pilot study of human brain tissue post-magnetic resonance imaging: Information from the National Deep Brain Stimulation Brain Tissue Network (DBS-BTN) , 2011, NeuroImage.

[36]  Takashi Hanakawa,et al.  A novel composite targeting method using high-field magnetic resonance imaging for subthalamic nucleus deep brain stimulation. , 2009, Journal of neurosurgery.

[37]  G. Paxinos,et al.  Atlas of the Human Brain , 2000 .

[38]  Keyoumars Ashkan,et al.  Optimal MRI methods for direct stereotactic targeting of the subthalamic nucleus and globus pallidus , 2010, European Radiology.

[39]  M. Kringelbach,et al.  Translational principles of deep brain stimulation , 2007, Nature Reviews Neuroscience.

[40]  Niels Sunde,et al.  Effects of bilateral stimulation of the subthalamic nucleus in patients with severe Parkinson's disease and motor fluctuations , 2002, Movement disorders : official journal of the Movement Disorder Society.

[41]  Marwan Hariz,et al.  Long‐term efficacy of thalamic deep brain stimulation for tremor: Double‐blind assessments , 2003, Movement disorders : official journal of the Movement Disorder Society.

[42]  John S. Thornton,et al.  High resolution MR anatomy of the subthalamic nucleus: Imaging at 9.4T with histological validation , 2012, NeuroImage.

[43]  Carlo Ciulla,et al.  Establishing a baseline phase behavior in magnetic resonance imaging to determine normal vs. abnormal iron content in the brain , 2007, Journal of magnetic resonance imaging : JMRI.

[44]  Benoit M. Dawant,et al.  Effect of MR Distortion on Targeting for Deep-Brain Stimulation , 2010, IEEE Transactions on Biomedical Engineering.

[45]  W. D. den Dunnen,et al.  Anatomical alterations of the subthalamic nucleus in relation to age: A postmortem study , 2005, Movement disorders : official journal of the Movement Disorder Society.

[46]  G Rees Cosgrove,et al.  Experience with Microelectrode Guided Subthalamic Nucleus Deep Brain Stimulation , 2006, Neurosurgery.

[47]  K V Slavin,et al.  Direct visualization of the human subthalamic nucleus with 3T MR imaging. , 2006, AJNR. American journal of neuroradiology.

[48]  J. Strzelczyk The Essential Physics of Medical Imaging , 2003 .

[49]  S. T. G. Roup,et al.  DEEP-BRAIN STIMULATION OF THE SUBTHALAMIC NUCLEUS OR THE PARS INTERNA OF THE GLOBUS PALLIDUS IN PARKINSON'S DISEASE , 2001 .

[50]  V A Coenen,et al.  Localization of the Subthalamic Nucleus: Optimization with Susceptibility-Weighted Phase MR Imaging , 2009, American Journal of Neuroradiology.

[51]  J. Boone,et al.  Comprar Essential Physics Of Medical Imaging, International Edition | Jerrold T. Bushberg | 9781451118100 | Lippincott Williams & Wilkins , 2012 .

[52]  B. Hallgren,et al.  THE EFFECT OF AGE ON THE NON‐HAEMIN IRON IN THE HUMAN BRAIN , 1958, Journal of neurochemistry.

[53]  Zhou Xiaoping,et al.  Risks of intracranial hemorrhage in patients with Parkinson's disease receiving deep brain stimulation and ablation. , 2010, Parkinsonism & related disorders.

[54]  J. R. Landis,et al.  An application of hierarchical kappa-type statistics in the assessment of majority agreement among multiple observers. , 1977, Biometrics.

[55]  J. Yelnik Functional anatomy of the basal ganglia , 2002, Movement disorders : official journal of the Movement Disorder Society.

[56]  M. Hariz,et al.  Variability of the subthalamic nucleus: The case for direct MRI guided targeting , 2007, British journal of neurosurgery.

[57]  Gareth J. Barker,et al.  Segmentation of the thalamus in MRI based on T1 and T2 , 2011, NeuroImage.

[58]  Bram Platel,et al.  Magnetic resonance imaging techniques for visualization of the subthalamic nucleus. , 2011, Journal of neurosurgery.

[59]  P. Chinnery,et al.  Neurodegeneration with brain iron accumulation. , 2011, Handbook of clinical neurology.

[60]  P. Krack,et al.  Deep brain stimulation: from neurology to psychiatry? , 2010, Trends in Neurosciences.

[61]  David Eidelberg,et al.  Metabolic brain networks associated with cognitive function in Parkinson's disease , 2007, NeuroImage.

[62]  Markus Barth,et al.  Nonnvasive assessment of vascular architecture and function during modulated blood oxygenation using susceptibility weighted magnetic resonance imaging , 2005, Magnetic resonance in medicine.

[63]  G. Schaltenbrand,et al.  Atlas for Stereotaxy of the Human Brain , 1977 .

[64]  S. Chung,et al.  Analysis of hemorrhagic risk factors during deep brain stimulation surgery for movement disorders: comparison of the circumferential paired and multiple electrode insertion methods , 2011, Acta Neurochirurgica.

[65]  P. Krack,et al.  Deep-brain stimulation of the subthalamic nucleus or the pars interna of the globus pallidus in Parkinson's disease. , 2001, The New England journal of medicine.

[66]  V. Visser-Vandewalle,et al.  SINGLE ELECTRODE AND MULTIPLE ELECTRODE GUIDED ELECTRICAL STIMULATION OF THE SUBTHALAMIC NUCLEUS IN ADVANCED PARKINSON'S DISEASE , 2007, Neurosurgery.

[67]  Lars Gerigk,et al.  Visualization of the internal globus pallidus: sequence and orientation for deep brain stimulation using a standard installation protocol at 3.0 Tesla , 2012, Acta Neurochirurgica.

[68]  P. Dechent,et al.  Improved Visibility of the Subthalamic Nucleus on High-Resolution Stereotactic MR Imaging by Added Susceptibility (T2*) Contrast Using Multiple Gradient Echoes , 2007, American Journal of Neuroradiology.

[69]  Vincent Dousset,et al.  Lack of agreement between direct magnetic resonance imaging and statistical determination of a subthalamic target: the role of electrophysiological guidance. , 2002, Journal of neurosurgery.

[70]  M I Hariz,et al.  A comparative study on ventriculographic and computerized tomography-guided determinations of brain targets in functional stereotaxis. , 1990, Journal of neurosurgery.

[71]  Essa Yacoub,et al.  Feasibility of Using Ultra-High Field (7 T) MRI for Clinical Surgical Targeting , 2012, PloS one.

[72]  Toshinori Hirai,et al.  Human subthalamic nucleus: evaluation with high-resolution MR imaging at 3.0 T , 2008, Neuroradiology.

[73]  J. R. Landis,et al.  The measurement of observer agreement for categorical data. , 1977, Biometrics.

[74]  R A Knight,et al.  MR imaging of human brain at 3.0 T: preliminary report on transverse relaxation rates and relation to estimated iron content. , 1999, Radiology.

[75]  John T. Gale,et al.  RISK FACTORS FOR HEMORRHAGE DURING MICROELECTRODE‐GUIDED DEEP BRAIN STIMULATION AND THE INTRODUCTION OF AN IMPROVED MICROELECTRODE DESIGN , 2009, Neurosurgery.

[76]  S. Paek,et al.  The Benefit of Subthalamic Deep Brain Stimulation for Pain in Parkinson Disease: A 2-Year Follow-up Study , 2012, Neurosurgery.

[77]  A. Shmuel,et al.  Imaging brain function in humans at 7 Tesla , 2001, Magnetic resonance in medicine.

[78]  Clement Hamani,et al.  Correspondence of microelectrode mapping with magnetic resonance imaging for subthalamic nucleus procedures. , 2005, Surgical neurology.

[79]  Anna Barnes,et al.  Network modulation by the subthalamic nucleus in the treatment of Parkinson's disease , 2006, NeuroImage.

[80]  Jeff H. Duyn,et al.  High-field MRI of brain cortical substructure based on signal phase , 2007, Proceedings of the National Academy of Sciences.

[81]  I. Hamada,et al.  Hemorrhagic complication of stereotactic surgery in patients with movement disorders. , 2003, Journal of neurosurgery.