Subcortical injury is an independent predictor of worsening neurological deficits following awake craniotomy procedures.

BACKGROUND Tailored craniotomies for awake procedures limit cortical exposure. Recently we demonstrated that the identification of eloquent areas increased the risk of postoperative deficits. However, it was not clear whether the observed neurological deficits were caused by proximity of functional cortex to the tumor [cortical injury] or subcortical injury. OBJECTIVE We hypothesize that subcortical injury during tumor resection is an important predictor of postoperative neurological deficits compared to cortical injury. METHODS A retrospective review of 214 patients undergoing awake craniotomy was carried out in whom preoperative functional magnetic resonance imaging (fMRI) and cortical mapping (CM) were performed. A radiologist blinded to the clinical data reviewed and graded the postoperative changes on diffusion-weighted MR-imaging (DWI). RESULTS Of the 40 cases who developed new intraoperative neurological deficit, 36 (90%) occurred during subcortical dissection, 3 (7.5%) during both subcortical and cortical dissection, and 1 (2.5%) during cortical dissection. Neurological dysfunction acquired during subcortical dissection was an independent predictor of postoperative deficits both in the immediate postoperative period (P < .001) and at the 3-month follow-up (P < .001). Significant DWI restriction in the subcortical white matter was predictive of neurological deficits both immediately and at 3 months, P = .011 and P < .001, respectively. New or worsening deficits were seen in 38% of patients; however, at 3 months 13% had a mild persistent neurological deficit. CONCLUSION Subcortical injury with significant DWI changes result in postoperative neurological decline despite our efforts to preserve cortical areas of function. This underscores the importance of preserving subcortical fiber tracts during awake craniotomy procedures.

[1]  G. Krol,et al.  Use of diffusion weighted magnetic resonance imaging in predicting early postoperative outcome of new neurological deficits after brain tumor resection. , 2006, Neurosurgery.

[2]  Costanza Papagno,et al.  Is Preoperative Functional Magnetic Resonance Imaging Reliable for Language Areas Mapping in Brain Tumor Surgery? Review of Language Functional Magnetic Resonance Imaging and Direct Cortical Stimulation Correlation Studies , 2010, Neurosurgery.

[3]  U. D. Schmid,et al.  Safe surgery of lesions near the motor cortex using intra-operative mapping techniques: a report on 50 patients , 2005, Acta Neurochirurgica.

[4]  S. Ronner,et al.  Cortical mapping for defining the limits of tumor resection. , 1987, Neurosurgery.

[5]  M. Berger,et al.  Functional mapping-guided resection of low-grade gliomas. , 1995, Clinical neurosurgery.

[6]  Mitchel S. Berger,et al.  Low grade gliomas: Functional mapping resection strategies, extent of resection, and outcome , 1997, Journal of Neuro-Oncology.

[7]  Mitchel S Berger,et al.  Functional outcome after language mapping for glioma resection. , 2008, The New England journal of medicine.

[8]  G. Ojemann,et al.  Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. 1989. , 2008, Journal of neurosurgery.

[9]  I. Fried,et al.  The asleep-awake-asleep anesthetic technique for intraoperative language mapping. , 1998, Neurosurgery.

[10]  W. Curry,et al.  Surgery for primary supratentorial brain tumors in the United States, 1988 to 2000: the effect of provider caseload and centralization of care. , 2005, Neuro-oncology.

[11]  M. Bernstein,et al.  Awake craniotomy with brain mapping as the routine surgical approach to treating patients with supratentorial intraaxial tumors: a prospective trial of 200 cases. , 1999, Journal of neurosurgery.

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

[13]  M. Albert,et al.  Severe nonfluency in aphasia. Role of the medial subcallosal fasciculus and other white matter pathways in recovery of spontaneous speech. , 1989, Brain : a journal of neurology.

[14]  Mitchel S. Berger,et al.  Cortical localization of temporal lobe language sites in patients with gliomas. , 1994 .

[15]  Wilhelm Eisner,et al.  Surgical Resection of Grade II Astrocytomas in the Superior Frontal Gyrus , 2002, Neurosurgery.

[16]  G. Ojemann,et al.  Cortical language localization in left, dominant hemisphere. An electrical stimulation mapping investigation in 117 patients. , 1989, Journal of neurosurgery.

[17]  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.

[18]  H. Duffau,et al.  Intraoperative subcortical stimulation mapping of language pathways in a consecutive series of 115 patients with Grade II glioma in the left dominant hemisphere. , 2008, Journal of neurosurgery.

[19]  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.

[20]  C. Papagno,et al.  INTRAOPERATIVE SUBCORTICAL LANGUAGETRACT MAPPING GUIDES SURGICAL REMOVALOF GLIOMAS INVOLVING SPEECH AREAS , 2007, Neurosurgery.

[21]  Susan M. Chang,et al.  Serial diffusion-weighted magnetic resonance imaging in cases of glioma: distinguishing tumor recurrence from postresection injury. , 2005, Journal of neurosurgery.

[22]  K R Hess,et al.  Neurosurgical outcomes in a modern series of 400 craniotomies for treatment of parenchymal tumors. , 1998, Neurosurgery.

[23]  Ganesh Rao,et al.  Intraoperative magnetic resonance imaging-guided tractography with integrated monopolar subcortical functional mapping for resection of brain tumors. Clinical article. , 2011, Journal of neurosurgery.

[24]  Pratik Mukherjee,et al.  Diffusion-tensor imaging-guided tracking of fibers of the pyramidal tract combined with intraoperative cortical stimulation mapping in patients with gliomas. , 2004, Journal of neurosurgery.

[25]  H. Duffau,et al.  Awake Mapping Optimizes the Extent of Resection for Low‐Grade Gliomas in Eloquent Areas , 2010, Neurosurgery.

[26]  R. Gonzalez,et al.  Diffusion-weighted imaging in acute stroke. , 2005, Neuroimaging clinics of North America.

[27]  Mitchel S Berger,et al.  Intraoperative subcortical stimulation mapping for hemispherical perirolandic gliomas located within or adjacent to the descending motor pathways: evaluation of morbidity and assessment of functional outcome in 294 patients. , 2004, Journal of neurosurgery.

[28]  F. Barker Craniotomy for the resection of metastatic brain tumors in the U.S., 1988–2000 , 2004, Cancer.

[29]  Kenji Ino,et al.  Combined use of tractography-integrated functional neuronavigation and direct fiber stimulation. , 2005, Journal of neurosurgery.