Functional Magnetic Resonance Imaging and Diffusion Tensor Tractography Incorporated Into an Intraoperative 3‐Dimensional Ultrasound‐Based Neuronavigation System: Impact on Therapeutic Strategies, Extent of Resection, and Clinical Outcome

BACKGROUNDFunctional neuronavigation with intraoperative 3-dimensional (3D) ultrasound may facilitate safer brain lesion resections than conventional neuronavigation. OBJECTIVEIn this study, functional magnetic resonance imaging (fMRI) and diffusion tensor tractography (DTT) were used to map eloquent areas. We assessed the use of fMRI and DTT for preoperative assessments and determined whether using these data together with 3D ultrasound during surgery enabled safer lesion resection. METHODSWe reviewed 51 consecutive patients with intracranial lesions in whom fMRI with or without DTT was used to map eloquent areas. To assess a possible impact of fMRI/DTT, we reviewed and analyzed the quality of the fMRI/DTT data, any change in therapeutic strategies, lesion to eloquent area distance (LEAD), extent of resection, and clinical outcome. RESULTSAs a result of the fMRI/DTT mapping, the therapeutic strategies were changed in 4 patients. The median tumor residue for glioma patients was 11% (n = 33) and 0% for nonglioma lesions (n = 12). For gliomas, there was a significant correlation between decreasing LEAD and increasing tumor residue. Of the glioma patients, 42% underwent gross total resection (≥ 95%) and 12% suffered neurological worsening after surgery as a result of complications. Of glioma patients with an LEAD of ≤ 5 mm, 24% underwent gross total resection and 10% experienced neurological deterioration. CONCLUSIONThis study demonstrates that preoperative fMRI and DTT had direct consequences for therapeutic strategies and indicates their impact on intraoperative strategies to spare eloquent cortex and tracts. Functional neuronavigation combined with intraoperative 3D ultrasound can, in most patients, enable resection of brain lesions with general anesthesia without jeopardizing neurological function.

[1]  Stefan Sunaert,et al.  Presurgical planning for tumor resectioning , 2006, Journal of magnetic resonance imaging : JMRI.

[2]  J. Møller,et al.  DIAGNOSIS OF VENTRICULAR DRAINAGE‐RELATED BACTERIAL MENINGITIS BY BROAD‐RANGE REAL‐TIME POLYMERASE CHAIN REACTION , 2007, Neurosurgery.

[3]  M. Catani,et al.  Diffusion-based tractography in neurological disorders: concepts, applications, and future developments , 2008, The Lancet Neurology.

[4]  R. Barnard,et al.  The classification of tumours of the central nervous system. , 1982, Neuropathology and applied neurobiology.

[5]  Giuseppe Scotti,et al.  Motor and language DTI Fiber Tracking combined with intraoperative subcortical mapping for surgical removal of gliomas , 2008, NeuroImage.

[6]  F. Lindseth,et al.  SonoWand, an Ultrasound-based Neuronavigation System , 2000, Neurosurgery.

[7]  G. Unsgaard,et al.  Surgical Resection of High-grade Gliomas in Eloquent Regions Guided by Blood Oxygenation Level Dependent Functional Magnetic Resonance Imaging, Diffusion Tensor Tractography, and Intraoperative Navigated 3D Ultrasound , 2009, Minimally invasive neurosurgery : MIN.

[8]  Ying Mao,et al.  CLINICAL EVALUATION AND FOLLOW‐UP OUTCOME OF DIFFUSION TENSOR IMAGING‐BASED FUNCTIONAL NEURONAVIGATION: A PROSPECTIVE, CONTROLLED STUDY IN PATIENTS WITH GLIOMAS INVOLVING PYRAMIDAL TRACTS , 2007, Neurosurgery.

[9]  Wen Qin,et al.  Diffusion tensor tractography in patients with cerebral tumors: a helpful technique for neurosurgical planning and postoperative assessment. , 2005, European journal of radiology.

[10]  Max A. Viergever,et al.  Brain shift estimation in image-guided neurosurgery using 3-D ultrasound , 2005, IEEE Transactions on Biomedical Engineering.

[11]  T. B. Müller,et al.  Intra-operative 3D ultrasound in neurosurgery , 2006, Acta Neurochirurgica.

[12]  C. Nimsky,et al.  Implementation of Fiber Tract Navigation , 2006, Neurosurgery.

[13]  Andreas Raabe,et al.  Functional Magnetic Resonance Imaging-integrated Neuronavigation: Correlation between Lesion-to-Motor Cortex Distance and Outcome , 2004, Neurosurgery.

[14]  B. Scheithauer,et al.  The 2007 WHO classification of tumours of the central nervous system , 2007, Acta Neuropathologica.

[15]  Susumu Mori,et al.  Fiber tracking: principles and strategies – a technical review , 2002, NMR in biomedicine.

[16]  R A Bakay,et al.  The EasyGuide Neuro image-guided surgery system. , 1997, Neurosurgery.

[17]  Christopher Nimsky,et al.  Intraoperative diffusion-tensor MR imaging: shifting of white matter tracts during neurosurgical procedures--initial experience. , 2005, Radiology.

[18]  Volker A Coenen,et al.  Preoperative assessment of motor cortex and pyramidal tracts in central cavernoma employing functional and diffusion-weighted magnetic resonance imaging. , 2002, Surgical neurology.

[19]  C. Lumenta,et al.  BrainLab VectorVision Neuronavigation System: technology and clinical experiences in 131 cases. , 1999, Neurosurgery.

[20]  G. Unsgaard,et al.  Functional neuronavigation combined with intra-operative 3D ultrasound: Initial experiences during surgical resections close to eloquent brain areas and future directions in automatic brain shift compensation of preoperative data , 2007, Acta Neurochirurgica.

[21]  M. Ferrante,et al.  Role of magnetic resonance tractography in the preoperative planning and intraoperative assessment of patients with intra-axial brain tumours , 2007, La radiologia medica.

[22]  Alexandra Golby,et al.  FUNCTIONAL BRAIN MAPPING AND ITS APPLICATIONS TO NEUROSURGERY , 2007, Neurosurgery.

[23]  K. Slavin.  Neuronavigation in neurosurgery: current state of affairs , 2008, Expert review of medical devices.

[24]  J. Lagopoulos,et al.  Mapping the primary motor cortex in healthy subjects and patients with peri-rolandic brain lesions before neurosurgery , 2008, Neurological research.

[25]  F. Lindseth,et al.  Accuracy evaluation of a 3D ultrasound-based neuronavigation system. , 2002, Computer aided surgery : official journal of the International Society for Computer Aided Surgery.

[26]  A. Bizzi,et al.  Presurgical functional MR imaging of language and motor functions: validation with intraoperative electrocortical mapping. , 2008, Radiology.

[27]  Susan Bookheimer,et al.  Pre-Surgical Language Mapping with Functional Magnetic Resonance Imaging , 2007, Neuropsychology Review.

[28]  Ernst Nennig,et al.  Localizing and lateralizing language in patients with brain tumors: feasibility of routine preoperative functional MR imaging in 81 consecutive patients. , 2007, Radiology.

[29]  Manbir Singh,et al.  Functional magnetic resonance imaging for brain mapping in neurosurgery. , 2003, Neurosurgical focus.

[30]  I D Wilkinson,et al.  Motor functional MRI for pre-operative and intraoperative neurosurgical guidance. , 2003, The British journal of radiology.

[31]  K Willmes,et al.  Functional MRI for presurgical planning: problems, artefacts, and solution strategies , 2001, Journal of neurology, neurosurgery, and psychiatry.

[32]  M. Berger,et al.  GLIOMA EXTENT OF RESECTION AND ITS IMPACT ON PATIENT OUTCOME , 2008, Neurosurgery.

[33]  Geirmund Unsgård,et al.  Preoperative Blood Oxygen Level-dependent Functional Magnetic Resonance Imaging in Patients with Primary Brain Tumors: Clinical Application and Outcome , 2004, Neurosurgery.

[34]  J G Ojemann,et al.  Preserved function in brain invaded by tumor. , 1996, Neurosurgery.

[35]  Nicolas Foroglou,et al.  Intra-operative MRI (iop-MR) for brain tumour surgery , 2009, British journal of neurosurgery.

[36]  Veit Rohde,et al.  Sequential Visualization of Brain and Fiber Tract Deformation during Intracranial Surgery with Three-dimensional Ultrasound: An Approach to Evaluate the Effect of Brain Shift , 2005, Neurosurgery.

[37]  N. Hata,et al.  Serial Intraoperative Magnetic Resonance Imaging of Brain Shift , 2001, Neurosurgery.

[38]  A. Heimberger,et al.  AWAKE CRANIOTOMY FOR BRAIN TUMORS NEAR ELOQUENT CORTEX: CORRELATION OF INTRAOPERATIVE CORTICAL MAPPING WITH NEUROLOGICAL OUTCOMES IN 309 CONSECUTIVE PATIENTS , 2009, Neurosurgery.