Testing the Reliability of BOLD-fMRI Motor Mapping in Patients with Cerebral Arteriovenous Malformations by Electric Cortical Stimulation and Surgery Outcomes.

OBJECTIVE To test the reliability of blood oxygenation level-dependent functional magnetic resonance imaging (fMRI) in the primary hand motor cortex (M1) among patients with arteriovenous malformations (AVMs) by electric cortical stimulation (ECS) and surgery outcomes. METHODS Forty-three patients with AVMs involving/adjacent to M1 underwent blood oxygen level-dependent fMRI (BOLD-fMRI) with repetitive finger-to-thumb opposition movements. The generated image sets were processed on the iPlan 3.0 workstation. A site-by-site comparison between the fMRI and ECS maps was performed with the aid of neuronavigation. Surgical outcomes were analyzed as the change between preoperative and postoperative muscle strength (MS). Finally, fMRI sensitivity was calculated, and correlations of lesion-to-activation distances (LAD) and surgery outcomes were analyzed. RESULTS The highest activation location was found in the ipsilateral M1in 40 patients (93%). The highest activation relocated in the contralateral M1area in one patient (2.3%). No motor activation was found in the other 2 (4.7%) patients. ECS results were positive in 34 patients (85%, 34/40). The fMRI sensitivity was calculated as 85%. In total, 18 patients (41.9%) had worsened MS 1 week after surgery. Eight patients (18.6%) suffered from permanent muscle strength deterioration 6 months later. Moreover, an LAD ≤5 mm was significantly associated with permanent MS deterioration (P = 0.039). CONCLUSION BOLD-fMRI exhibits high sensitivity in motor mapping in patients with AVMs. LAD ≤5 mm may be associated with permanent MS deterioration in patients with AVM close to the motor cortex.

[1]  C. Braun,et al.  Misleading functional magnetic resonance imaging mapping of the cortical hand representation in a 4-year-old boy with an arteriovenous malformation of the central region. , 2009, Journal of neurosurgery. Pediatrics.

[2]  Jean-Christophe Sol,et al.  Quantification of True In Vivo (Application) Accuracy in Cranial Image-guided Surgery: Influence of Mode of Patient Registration , 2006, Neurosurgery.

[3]  Giancarlo Ferrigno,et al.  BOLD fMRI integration into radiosurgery treatment planning of cerebral vascular malformations. , 2007, Medical physics.

[4]  C. Ogilvy,et al.  Brain Mapping for Safe Microsurgical Resection of Arteriovenous Malformations in Eloquent Cortex. , 2015, World neurosurgery.

[5]  A. Falini,et al.  Intraoperative mapping for tumor resection. , 2009, Neuroimaging clinics of North America.

[6]  Michael Buchfelder,et al.  Integration of functional neuronavigation and intraoperative MRI in surgery for drug-resistant extratemporal epilepsy close to eloquent brain areas. , 2013, Neurosurgical focus.

[7]  M. Morgan,et al.  How Safe Is Arteriovenous Malformation Surgery? A Prospective, Observational Study of Surgery As First‐Line Treatment for Brain Arteriovenous Malformations , 2010, Neurosurgery.

[8]  Stéphane Lehéricy,et al.  Arteriovenous brain malformations: is functional MR imaging reliable for studying language reorganization in patients? Initial observations. , 2002, Radiology.

[9]  Brittany M. Young,et al.  Characterizing the relationship between functional MRI-derived measures and clinical outcomes in patients with vascular lesions. , 2013, Neurosurgical focus.

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

[11]  Wade M Mueller,et al.  Lesion-induced Pseudo-dominance at Functional Magnetic Resonance Imaging: Implications for Preoperative Assessments , 2004, Neurosurgery.

[12]  H. Freund,et al.  Restorative neurosurgery of the cortex: resections of pathologies of the central area can improve preexisting motor deficits , 2012, Neurosurgical Review.

[13]  G. Schroth,et al.  Whole-brain functional magnetic resonance imaging of cerebral arteriovenous malformations involving the motor pathways , 2002, Neuroradiology.

[14]  V. Seifert,et al.  Intraoperative Risk of Seizures Associated With Transient Direct Cortical Stimulation in Patients With Symptomatic Epilepsy , 2007, Journal of clinical neurophysiology : official publication of the American Electroencephalographic Society.

[15]  T. Nägele,et al.  Safe Resection of Arteriovenous Malformations in Eloquent Motor Areas Aided by Functional Imaging and Intraoperative Monitoring , 2012, Neurosurgery.

[16]  Y. Sitoh,et al.  Cortical reorganization of motor functional areas in cerebral arteriovenous malformations , 2013, Journal of Clinical Neuroscience.

[17]  R. Du,et al.  Natural history of cerebral arteriovenous malformations: a meta-analysis. , 2013, Journal of neurosurgery.

[18]  Nader Pouratian,et al.  Functional Magnetic Resonance Imaging and Optical Imaging for Dominant-hemisphere Perisylvian Arteriovenous Malformations , 2004, Neurosurgery.

[19]  I. Berry,et al.  Methodological and Technical Issues for Integrating Functional Magnetic Resonance Imaging Data in a Neuronavigational System , 2001, Neurosurgery.

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

[21]  Shuo Wang,et al.  Functional MRI-guided microsurgery of intracranial arteriovenous malformations: study protocol for a randomised controlled trial , 2014, BMJ Open.

[22]  A. Algra,et al.  Treatment of Brain Arteriovenous Malformations: A Systematic Review and Meta-Analysis , 2012 .

[23]  A Olivier,et al.  Presurgical motor and somatosensory cortex mapping with functional magnetic resonance imaging and positron emission tomography. , 1999, Journal of neurosurgery.

[24]  R. Cox,et al.  Functional MR activation correlated with intraoperative cortical mapping. , 1997, AJNR. American journal of neuroradiology.

[25]  S S Kollias,et al.  Intraoperative validation of functional magnetic resonance imaging and cortical reorganization patterns in patients with brain tumors involving the primary motor cortex. , 1999, Journal of neurosurgery.

[26]  M. McDermott,et al.  Language and Motor Mapping During Resection of Brain Arteriovenous Malformations: Indications, Feasibility, and Utility , 2011, Neurosurgery.

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

[28]  Dietmar Frey,et al.  Functional brain mapping of patients with arteriovenous malformations using navigated transcranial magnetic stimulation: first experience in ten patients , 2014, Acta Neurochirurgica.

[29]  D P Auer,et al.  Neuronavigation and functional MRI for surgery in patients with lesion in eloquent brain areas. , 2002, Minimally invasive neurosurgery : MIN.

[30]  A. Rhoton,et al.  Arteriovenous malformations of the basal ganglia region: Rationale for surgical management , 2007, Acta Neurochirurgica.

[31]  Spyros S. Kollias,et al.  Intraoperative validation of functional magnetic resonance imaging and cortical reorganization patterns in patients with brain tumors involving the primary motor cortex , 1999 .

[32]  H. Alkadhi,et al.  Localization of the motor hand area to a knob on the precentral gyrus. A new landmark. , 1997, Brain : a journal of neurology.

[33]  H Uchida,et al.  Identification of pre- and postcentral gyri on CT and MR images on the basis of the medullary pattern of cerebral white matter. , 1991, Radiology.

[34]  M. Lawton,et al.  Multimodality treatment of deep arteriovenous malformations: thalamus, basal ganglia, and brain stem. , 1995, Neurosurgery.

[35]  B. Kundu,et al.  Impact of Brain Tumor Location on Morbidity and Mortality: A Retrospective Functional MR Imaging Study , 2011, American Journal of Neuroradiology.

[36]  Dong Wang,et al.  Intraoperative MRI with integrated functional neuronavigation-guided resection of supratentorial cavernous malformations in eloquent brain areas , 2011, Journal of Clinical Neuroscience.