Predicting brain tumor regrowth in relation to motor areas by functional brain mapping.

Background Due to frequent recurrences, high-grade gliomas still confer a poor prognosis. Several regrowth prediction models have been developed, but most of these models are based on cellular models or dynamic mathematical calculations, thus limiting direct clinical use. The present study aims to evaluate whether navigated transcranial magnetic stimulation (nTMS) or functional magnetic resonance imaging (fMRI) may be used to predict the direction of tumor regrowth. Methods Sixty consecutive patients with high-grade gliomas were enrolled prospectively and analyzed in a case-control design after tumor recurrence. All patients underwent serial MRI after surgery and suffered from recurrent tumors during a mean follow-up of 13.2 ± 14.9 months. Tumor regrowth speed and direction were measured in relation to motor areas defined by nTMS, nTMS-based tractography, and fMRI. Depending on initial resection, patients were separated into three groups (group 1: without residual tumor, group 2: residual tumor away from motor areas, and group 3: residual tumor facing motor areas). Results Sixty-nine percent of patients in group 1, 64.3% in group 2, and 66.7% in group 3 showed tumor recurrence towards motor eloquence on contrast-enhanced T1-weighted sequences (P = .9527). Average growth towards motor areas on contrast-enhanced T1-weighted sequences was 0.6 ± 1.5 (group 1), 0.6 ± 2.4 (group 2), and 2.3 ± 5.5 (group 3) mm/month (P = .0492). Conclusion This study suggests a new strategy to predict tumor regrowth patterns in high-grade glioma patients. Our approach could be directly applied in the clinical setting, thus having clinical impact on both surgical treatment and radiotherapy planning. Ethics Committee Registration Number 2793/10.

[1]  B. Meyer,et al.  Implementing Functional Preoperative Mapping in the Clinical Routine of a Neurosurgical Department: Technical Note. , 2017, World neurosurgery.

[2]  Kyung K Peck,et al.  Brain Tumors: The Influence of Tumor Type and Routine MR Imaging Characteristics at BOLD Functional MR Imaging in the Primary Motor Gyrus. , 2016, Radiology.

[3]  R. Sawaya,et al.  Technical principles in glioma surgery and preoperative considerations , 2016, Journal of Neuro-Oncology.

[4]  Q. Long,et al.  Mathematical Modelling of a Brain Tumour Initiation and Early Development: A Coupled Model of Glioblastoma Growth, Pre-Existing Vessel Co-Option, Angiogenesis and Blood Perfusion , 2016, PloS one.

[5]  Jingyuan E. Chen,et al.  Functional Magnetic Resonance Imaging Methods , 2015, Neuropsychology Review.

[6]  Rüdiger Hilker,et al.  Does navigated transcranial stimulation increase the accuracy of tractography? A prospective clinical trial based on intraoperative motor evoked potential monitoring during deep brain stimulation. , 2015, Neurosurgery.

[7]  Hechun Xia,et al.  Integration of BOLD-fMRI and DTI into radiation treatment planning for high-grade gliomas located near the primary motor cortexes and corticospinal tracts , 2015, Radiation Oncology.

[8]  Christian Grefkes,et al.  Improved nTMS- and DTI-derived CST tractography through anatomical ROI seeding on anterior pontine level compared to internal capsule , 2015, NeuroImage: Clinical.

[9]  Francesco Tomasello,et al.  Navigated Transcranial Magnetic Stimulation for “Somatotopic” Tractography of the Corticospinal Tract , 2014, Neurosurgery.

[10]  J. Debus,et al.  Glioblastoma recurrence patterns after radiation therapy with regard to the subventricular zone. , 2014, International journal of radiation oncology, biology, physics.

[11]  C. Zimmer,et al.  Technical considerations on the validity of blood oxygenation level‐dependent‐based MR assessment of vascular deoxygenation , 2014, NMR in biomedicine.

[12]  P. Vajkoczy,et al.  Integration of navigated brain stimulation data into radiosurgical planning: potential benefits and dangers , 2014, Acta Neurochirurgica.

[13]  Christine Preibisch,et al.  MR-based hypoxia measures in human glioma , 2013, Journal of Neuro-Oncology.

[14]  Francesco Tomasello,et al.  Integration of functional neuroimaging in CyberKnife radiosurgery: feasibility and dosimetric results. , 2013, Neurosurgical focus.

[15]  Bernhard Meyer,et al.  Presurgical navigated transcranial magnetic brain stimulation for recurrent gliomas in motor eloquent areas , 2013, Clinical Neurophysiology.

[16]  H. Duffau,et al.  The “onco-functional balance” in surgery for diffuse low-grade glioma: integrating the extent of resection with quality of life , 2013, Acta Neurochirurgica.

[17]  Mitchel S Berger,et al.  Impact of extent of resection for recurrent glioblastoma on overall survival: clinical article. , 2012, Journal of neurosurgery.

[18]  P. Vajkoczy,et al.  A new approach for corticospinal tract reconstruction based on navigated transcranial stimulation and standardized fractional anisotropy values , 2012, NeuroImage.

[19]  Phiroz E. Tarapore,et al.  Preoperative multimodal motor mapping: a comparison of magnetoencephalography imaging, navigated transcranial magnetic stimulation, and direct cortical stimulation. , 2012, Journal of neurosurgery.

[20]  B. Meyer,et al.  Utility of presurgical navigated transcranial magnetic brain stimulation for the resection of tumors in eloquent motor areas. , 2012, Journal of neurosurgery.

[21]  Bernhard Meyer,et al.  Diffusion tensor imaging fiber tracking using navigated brain stimulation—a feasibility study , 2012, Acta Neurochirurgica.

[22]  Quan Long,et al.  Coupled modelling of tumour angiogenesis, tumour growth and blood perfusion. , 2011, Journal of theoretical biology.

[23]  Francesco Tomasello,et al.  Role of stereotactic radiosurgery and fractionated stereotactic radiotherapy for the treatment of recurrent glioblastoma multiforme. , 2009, Neurosurgical focus.

[24]  Peter Vajkoczy,et al.  NAVIGATED TRANSCRANIAL MAGNETIC STIMULATION FOR PREOPERATIVE FUNCTIONAL DIAGNOSTICS IN BRAIN TUMOR SURGERY , 2009, Neurosurgery.

[25]  R. McLendon,et al.  The hypoxic microenvironment maintains glioblastoma stem cells and promotes reprogramming towards a cancer stem cell phenotype , 2009, Cell cycle.

[26]  S. McDougall,et al.  Multiscale modelling and nonlinear simulation of vascular tumour growth , 2009, Journal of mathematical biology.

[27]  J. Debus,et al.  Radiochemotherapy in patients with primary glioblastoma comparing two temozolomide dose regimens. , 2008, International journal of radiation oncology, biology, physics.

[28]  U. Lendahl,et al.  Notch signaling mediates hypoxia-induced tumor cell migration and invasion , 2008, Proceedings of the National Academy of Sciences.

[29]  J. Debus,et al.  Postoperative treatment of primary glioblastoma multiforme with radiation and concomitant temozolomide in elderly patients. , 2008, International journal of radiation oncology, biology, physics.

[30]  Olivier Clatz,et al.  Biocomputing: numerical simulation of glioblastoma growth using diffusion tensor imaging , 2008, Physics in medicine and biology.

[31]  A. Brodbelt,et al.  ‘Recurrent’ glioblastoma multiforme, when should we reoperate? , 2008, British journal of neurosurgery.

[32]  J. Lowengrub,et al.  Nonlinear simulation of the effect of microenvironment on tumor growth. , 2007, Journal of theoretical biology.

[33]  Martin J. van den Bent,et al.  Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. , 2005, The New England journal of medicine.

[34]  Daniel J Brat,et al.  Pseudopalisades in Glioblastoma Are Hypoxic, Express Extracellular Matrix Proteases, and Are Formed by an Actively Migrating Cell Population , 2004, Cancer Research.

[35]  P. Maini,et al.  A cellular automaton model for tumour growth in inhomogeneous environment. , 2003, Journal of theoretical biology.

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

[37]  A. Kalnin,et al.  Functional magnetic resonance imaging aided radiation treatment planning. , 2000, Medical physics.

[38]  J Hennig,et al.  The influence of gliomas and nonglial space-occupying lesions on blood-oxygen-level-dependent contrast enhancement. , 2000, AJNR. American journal of neuroradiology.

[39]  M. Westphal,et al.  Migration of human glioma cells on myelin. , 1996, Neurosurgery.

[40]  Mitchel S. Berger,et al.  Current and future strategies for treatment of glioma , 2016, Neurosurgical Review.

[41]  M. Berger,et al.  Recent surgical management of gliomas. , 2012, Advances in experimental medicine and biology.