The Role of 3D Tractography in Skull Base Surgery: Technological Advances, Feasibility, and Early Clinical Assessment with Anterior Skull Base Meningiomas

Abstract

Objective The aim of this study is to determine feasibility of incorporating three-dimensional (3D) tractography into routine skull base surgery planning and analyze our early clinical experience in a subset of anterior cranial base meningiomas (ACM).

Methods Ninety-nine skull base endonasal and transcranial procedures were planned in 94 patients and retrospectively reviewed with a further analysis of the ACM subset.

Main Outcome Measures (1) Automated generation of 3D tractography; (2) co-registration 3D tractography with computed tomography (CT), CT angiography (CTA), and magnetic resonance imaging (MRI); and (3) demonstration of real-time manipulation of 3D tractography intraoperatively. ACM subset: (1) pre- and postoperative cranial nerve function, (2) qualitative assessment of white matter tract preservation, and (3) frontal lobe fluid-attenuated inversion recovery (FLAIR) signal abnormality.

Results Automated 3D tractography, with MRI, CT, and CTA overlay, was produced in all cases and was available intraoperatively. ACM subset: 8 (44%) procedures were performed via a ventral endoscopic endonasal approach (EEA) corridor and 12 (56%) via a dorsal anteromedial (DAM) transcranial corridor. Four cases (olfactory groove meningiomas) were managed with a combined, staged approach using ventral EEA and dorsal transcranial corridors. Average tumor volume reduction was 90.3 ± 15.0. Average FLAIR signal change was –30.9% ± 58.6. 11/12 (92%) patients (DAM subgroup) demonstrated preservation of, or improvement in, inferior fronto-occipital fasciculus volume. Functional cranial nerve recovery was 89% (all cases).

Conclusion It is feasible to incorporate 3D tractography into the skull base surgical armamentarium. The utility of this tool in improving outcomes will require further study.

Keywords

skull base surgery - neuronavigation - tractography - computed tomography - computed tomography angiography - magnetic resonance imaging - diffusion tensor imaging

Publication History

Received: 04 February 2020

Accepted: 25 April 2020

Article published online:
14 August 2020

• References

• 1 Bello L, Gambini A, Castellano A. et al. Motor and language DTI fiber tracking combined with intraoperative subcortical mapping for surgical removal of gliomas. Neuroimage 2008; 39 (01) 369-382
• 2 Wu JS, Zhou LF, Tang WJ. 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. Neurosurgery 2007; 61 (05) 935-948 , discussion 948–949
• 3 Abdullah KG, Lubelski D, Nucifora PG, Brem S. Use of diffusion tensor imaging in glioma resection. Neurosurg Focus 2013; 34 (04) E1 . Doi: 10.3171/2013.1.FOCUS12412
• 4 Nimsky C. Intraoperative acquisition of fMRI and DTI. Neurosurg Clin N Am 2011; 22 (02) 269-277 , ix
• 5 Witwer BP, Moftakhar R, Hasan KM. et al. Diffusion-tensor imaging of white matter tracts in patients with cerebral neoplasm. J Neurosurg 2002; 97 (03) 568-575
• 6 Romano A, D'Andrea G, Minniti G. et al. Pre-surgical planning and MR-tractography utility in brain tumour resection. Eur Radiol 2009; 19 (12) 2798-2808
• 7 Clark CA, Barrick TR, Murphy MM, Bell BA. White matter fiber tracking in patients with space-occupying lesions of the brain: a new technique for neurosurgical planning?. Neuroimage 2003; 20 (03) 1601-1608
• 8 Prevedello DM, Ditzel Filho LF, Fernandez-Miranda JC. et al. Magnetic resonance imaging fluid-attenuated inversion recovery sequence signal reduction after endoscopic endonasal transcribiform total resection of olfactory groove meningiomas. Surg Neurol Int 2015; 6: 158 . Doi: 10.4103/2152-7806.166846
• 9 Synaptive Medical. BrightMatterTM Plan. 2015.www.synaptivemedical.com/products/plan/
• 10 Chakravarthi S, Monroy-Sosa A, Gonen L. et al. Reanalyzing the “far medial” (transcondylar-transtubercular) approach based on three anatomical vectors: the ventral posterolateral corridor. J Neurosurg Sci 2018; 62 (03) 347-355
• 11 Kassam AB, Prevedello DM, Carrau RL. et al. The front door to Meckel's cave: an anteromedial corridor via expanded endoscopic endonasal approach- technical considerations and clinical series. Neurosurgery 2009;64(3, Suppl)ons71–ons82, discussion ons82–ons83. Doi: 10.1227/01.NEU.0000335162.36862.54
• 12 Kassam A, Snyderman CH, Mintz A, Gardner P, Carrau RL. Expanded endonasal approach: the rostrocaudal axis. Part I. Crista galli to the sella turcica. Neurosurg Focus 2005; 19 (01) E3
• 13 Kassam A, Snyderman CH, Mintz A, Gardner P, Carrau RL. Expanded endonasal approach: the rostrocaudal axis. Part II. Posterior clinoids to the foramen magnum. Neurosurg Focus 2005; 19 (01) E4
• 14 Gardner PA, Kassam AB, Thomas A. et al. Endoscopic endonasal resection of anterior cranial base meningiomas. Neurosurgery 2008; 63 (01) 36-52 , discussion 52–54
• 15 Rangel-Castilla L, Russin JJ, Spetzler RF. Surgical management of skull base tumors. Rep Pract Oncol Radiother 2016; 21 (04) 325-335
• 16 Komotar RJ, Starke RM, Raper DM, Anand VK, Schwartz TH. Endoscopic endonasal versus open transcranial resection of anterior midline skull base meningiomas. World Neurosurg 2012; 77 (5-6): 713-724
• 17 Schroeder HW. Indications and limitations of the endoscopic endonasal approach for anterior cranial base meningiomas. World Neurosurg 2014; 82 (6, Suppl): S81-S85
• 18 Yaşargil MG. A legacy of microneurosurgery: memoirs, lessons, and axioms. [Miscellaneous Article] Neurosurgery 1999; 45 (05) 1025-1092
• 19 Yasargil MG. Surgical concerns. In: Microneurosurgery. 3B. New York: Thieme; 1988: 25-53
• 20 de Almeida JR, Carvalho F, Vaz Guimaraes Filho F. et al. Comparison of endoscopic endonasal and bifrontal craniotomy approaches for olfactory groove meningiomas: a matched pair analysis of outcomes and frontal lobe changes on MRI. J Clin Neurosci 2015; 22 (11) 1733-1741
• 21 Bowers CA, Altay T, Couldwell WT. Surgical decision-making strategies in tuberculum sellae meningioma resection. Neurosurg Focus 2011; 30 (05) E1 . Doi: 10.3171/2011.2.FOCUS1115
• 22 de Divitiis E, Esposito F, Cappabianca P, Cavallo LM, de Divitiis O. Tuberculum sellae meningiomas: high route or low route? A series of 51 consecutive cases. Neurosurgery 2008; 62 (03) 556-563 , discussion 556–563
• 23 Kitano M, Taneda M, Nakao Y. Postoperative improvement in visual function in patients with tuberculum sellae meningiomas: results of the extended transsphenoidal and transcranial approaches. J Neurosurg 2007; 107 (02) 337-346
• 24 Fatemi N, Dusick JR, de Paiva Neto MA, Malkasian D, Kelly DF. Endonasal versus supraorbital keyhole removal of craniopharyngiomas and tuberculum sellae meningiomas. Neurosurgery 2009;64(05, Suppl 2):269–284, discussion 284–286
• 25 Ottenhausen M, Rumalla K, Alalade AF. et al. Decision-making algorithm for minimally invasive approaches to anterior skull base meningiomas. Neurosurg Focus 2018; 44 (04) E7 . Doi: 10.3171/2018.1.FOCUS17734
• 26 Bi WL, Abedalthagafi M, Horowitz P. et al. Genomic landscape of intracranial meningiomas. J Neurosurg 2016; 125 (03) 525-535
• 27 Aguiar PH, Tahara A, Almeida AN. et al. Olfactory groove meningiomas: approaches and complications. J Clin Neurosci 2009; 16 (09) 1168-1173
• 28 Bi WL, Dunn IF. Current and emerging principles in surgery for meningioma. Linchuang Zhongliuxue Zazhi 2017; 6 (Suppl. 01) S7 . Doi: 10.21037/cco.2017.06.10
• 29 Bassiouni H, Asgari S, Stolke D. Olfactory groove meningiomas: functional outcome in a series treated microsurgically. Acta Neurochir (Wien) 2007; 149 (02) 109-121 , discussion 121
• 30 Ciurea AV, Iencean SM, Rizea RE, Brehar FM. Olfactory groove meningiomas: a retrospective study on 59 surgical cases. Neurosurg Rev 2012; 35 (02) 195-202 , discussion 202
• 31 de Almeida JR, Carvalho F, Vaz Guimaraes Filho F. et al. Comparison of endoscopic endonasal and bifrontal craniotomy approaches for olfactory groove meningiomas: a matched pair analysis of outcomes and frontal lobe changes on MRI. J Clin Neurosci 2015; 22 (11) 1733-1741
• 32 Abbassy M, Woodard TD, Sindwani R, Recinos PF. An overview of anterior skull base meningiomas and the endoscopic endonasal approach. Otolaryngol Clin North Am 2016; 49 (01) 141-152
• 33 Di Maio S, Ramanathan D, Garcia-Lopez R. et al. Evolution and future of skull base surgery: the paradigm of skull base meningiomas. World Neurosurg 2012; 78 (3-4): 260-275
• 34 Brastianos PK, Horowitz PM, Santagata S. et al. Genomic sequencing of meningiomas identifies oncogenic SMO and AKT1 mutations. Nat Genet 2013; 45 (03) 285-289
• 35 Gunel M. , Yale-Bonn-Cologne Brain Tumor Genetics Study Group. 218 Meningioma Driver Mutations Determine Their Anatomical Site of Origin. Neurosurgery 2016; 63 (Suppl. 01) 185 . Doi: 10.1227/01.neu.0000489787.29664.ec
• 36 Byvalsev VA, Stepanov IA, Belykh EG, Yarullina AI. [Molecular biology of brain meningiomas]. Patol Fiziol Eksp Ter 2017; 61 (02) 82-91
• 37 Gonen L, Chakravarthi SS, Monroy-Sosa A. et al. Initial experience with a robotically operated video optical telescopic-microscope in cranial neurosurgery: feasibility, safety, and clinical applications. Neurosurg Focus 2017; 42 (05) E9 . Doi: 10.3171/2017.3.FOCUS1712
• 38 Snyderman CH, Pant H, Carrau RL, Prevedello D, Gardner P, Kassam AB. What are the limits of endoscopic sinus surgery?: the expanded endonasal approach to the skull base. Keio J Med 2009; 58 (03) 152-160
• 39 Prevedello DM, Thomas A, Gardner P, Snyderman CH, Carrau RL, Kassam AB. Endoscopic endonasal resection of a synchronous pituitary adenoma and a tuberculum sellae meningioma: technical case report. Neurosurgery 2007;60(04, Suppl 2):E401, discussion E401. Doi: 10.1227/01.NEU.0000255359.94571.91
• 40 Ditzel Filho LFS, Prevedello DM, Jamshidi AO. et al. Endoscopic endonasal approach for removal of tuberculum sellae meningiomas. Neurosurg Clin N Am 2015; 26 (03) 349-361