- Department of Computer Science, Washington University, St. Louis, Missouri, USA
- Department of Neurological Surgery, Washington University School of Medicine, St. Louis, Missouri, USA
- Department of Biomedical Engineering, Washington University, St. Louis, Missouri, USA
- Center for Innovation in Neuroscience and Technology, Washington University School of Medicine, St. Louis, Missouri, USA
Correspondence Address:
S. Kathleen Bandt
Department of Neurological Surgery, Washington University School of Medicine, St. Louis, Missouri, USA
Department of Biomedical Engineering, Washington University, St. Louis, Missouri, USA
Center for Innovation in Neuroscience and Technology, Washington University School of Medicine, St. Louis, Missouri, USA
DOI:10.4103/2152-7806.175885
Copyright: © 2016 Surgical Neurology International This is an open access article distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 3.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as the author is credited and the new creations are licensed under the identical terms.How to cite this article: Batra P, Bandt SK, Leuthardt EC. Resting state functional connectivity magnetic resonance imaging integrated with intraoperative neuronavigation for functional mapping after aborted awake craniotomy. Surg Neurol Int 05-Feb-2016;7:13
How to cite this URL: Batra P, Bandt SK, Leuthardt EC. Resting state functional connectivity magnetic resonance imaging integrated with intraoperative neuronavigation for functional mapping after aborted awake craniotomy. Surg Neurol Int 05-Feb-2016;7:13. Available from: http://surgicalneurologyint.com/surgicalint_articles/resting-state-functional-connectivity-magnetic-resonance-imaging-integrated-with-intraoperative-neuronavigation-for-functional-mapping-after-aborted-awake-craniotomy/
Abstract
Background:Awake craniotomy is currently the gold standard for aggressive tumor resections in eloquent cortex. However, a significant subset of patients is unable to tolerate this procedure, particularly the very young or old or those with psychiatric comorbidities, cardiopulmonary comorbidities, or obesity, among other conditions. In these cases, typical alternative procedures include biopsy alone or subtotal resection, both of which are associated with diminished surgical outcomes.
Case Description:Here, we report the successful use of a preoperatively obtained resting state functional connectivity magnetic resonance imaging (MRI) integrated with intraoperative neuronavigation software in order to perform functional cortical mapping in the setting of an aborted awake craniotomy due to loss of airway.
Conclusion:Resting state functional connectivity MRI integrated with intraoperative neuronavigation software can provide an alternative option for functional cortical mapping in the setting of an aborted awake craniotomy.
Keywords: Awake craniotomy, functional mapping, intraoperative neuronavigation, resting state functional connectivity magnetic resonance imaging
BACKGROUND
The goal of an awake craniotomy for tumor resection is to remove as much pathologic tissue as possible while preserving cortical structures subserving functions such as speech and motor control.[
CASE DESCRIPTION
Clinical history and physical examination
Our patient was a 57-year-old right-handed gentleman with a remote history of colon cancer who presented with increasing headache frequency and severity with new onset complex partial seizures. MRI identified a left posterior frontotemporal tumor suggestive of a high-grade glioma [
Figure 1
Preoperative anatomic magnetic resonance imaging. (a) Sagittal T1-weighted contrasted magnetic resonance imaging demonstrating a rim enhancing peri-sylvian mass consistent with primary glial neoplasm. (b) Axial fluid attenuated inversion recovery magnetic resonance imaging sequence demonstrating the same peri-sylvian mass with significant surrounding edema
Surgical procedure
The patient was placed in the three-quarter lateral position exposing the left side for craniotomy. He was mildly sedated with remifentanil and midazolam by the anesthesia team for surgical exposure. Supraorbital and posterior occipital nerve blocks were performed prior to fixing his head in an MRI compatible Mayfield cranial fixation device (Integra Life Sciences, Plainsboro NJ, USA). A circumferential field block was then performed, and the patient's head was coregistered with the intraoperative stereotactic navigation system (StealthStation, Medtronic, Inc., Minneapolis, MN, USA). Following coregistration, the surgical team was notified by anesthesia that the patient was vomiting and had aspirated, and they would need to place an endotracheal tube to protect the patient's airway moving forward. At this juncture, the following options were considered: Aborting the procedure, proceeding with biopsy alone or proceeding with surgical resection based on previously integrated preoperative resting state functional connectivity MRI.
The patient's preoperative resting state functional connectivity MRI suggested that there was a corridor through the parietal lobe that would allow for surgical resection without damage to adjacent eloquent cortex [Figures
CONCLUSION
Since its introduction in the 1990s, task-based fMRI has shown tremendous potential as an adjunctive tool to delineate areas of eloquent cortex for preoperative planning.[
Currently, the gold standard for mapping eloquent cortex for neurosurgical procedures involves ECS testing during an awake craniotomy.[
Preoperative fMRI has been extensively compared to intraoperative ECS, generally with favorable results.[
In conclusion, preoperative resting state functional connectivity MRI is a viable alternative for the management of eloquently located brain tumors when an awake craniotomy isn’t feasible or is poorly tolerated. Since resting state functional connectivity, MRI is both noninvasive and nonparticipatory, it is more broadly applicable than both task-based fMRI and awake ECS for mapping of the functional cortex. Its use for this purpose would allow tumor resections within eloquent cortex to be performed under a wider variety of circumstances. This, in turn, could lead to improved neurosurgical outcomes. The successful resection of our patient's left temporoparietal high-grade glioma using integrated preoperative fMRI instead of awake cortical stimulation in the setting of an aborted awake craniotomy supports the use of preoperatively acquired resting state functional connectivity MRI as an effective alternative to an awake cortical mapping.
Financial support and sponsorship
Nil.
Conflicts of interest
There are no conflicts of interest.
References
1. Ammirati M, Vick N, Liao YL, Ciric I, Mikhael M. Effect of the extent of surgical resection on survival and quality of life in patients with supratentorial glioblastomas and anaplastic astrocytomas. Neurosurgery. 1987. 21: 201-6
2. Berger MS. The impact of technical adjuncts in the surgical management of cerebral hemispheric low-grade gliomas of childhood. J Neurooncol. 1996. 28: 129-55
3. Bizzi A, Blasi V, Falini A, Ferroli P, Cadioli M, Danesi U. Presurgical functional MR imaging of language and motor functions: Validation with intraoperative electrocortical mapping. Radiology. 2008. 248: 579-89
4. Brown PD, Maurer MJ, Rummans TA, Pollock BE, Ballman KV, Sloan JA. A prospective study of quality of life in adults with newly diagnosed high-grade gliomas: The impact of the extent of resection on quality of life and survival. Neurosurgery. 2005. 57: 495-504
5. Buckner JC. Factors influencing survival in high-grade gliomas. Semin Oncol. 2003. 30: 10-4
6. Carrabba G, Venkatraghavan L, Bernstein M. Day surgery awake craniotomy for removing brain tumours: Technical note describing a simple protocol. Minim Invasive Neurosurg. 2008. 51: 208-10
7. Ciric I, Ammirati M, Vick N, Mikhael M. Supratentorial gliomas: Surgical considerations and immediate postoperative results.Gross total resection versus partial resection. Neurosurgery. 1987. 21: 21-6
8. Clark VP, Fannon S, Lai S, Benson R, Bauer L. Responses to rare visual target and distractor stimuli using event-related fMRI. J Neurophysiol. 2000. 83: 3133-9
9. Fadel NEldahab HWageh OWafik HLast accessed on 2013 Jun 18. Available from: http://www.onlinelibrary.wiley.com/o/cochrane/clcentral/articles/935/CN-00789935/frame.html .
10. Fadul C, Wood J, Thaler H, Galicich J, Patterson RH. , Posner JB.Morbidity and mortality of craniotomy for excision of supratentorial gliomas. Neurology. 1988. 38: 1374-9
11. Fox MD, Greicius M. Clinical applications of resting state functional connectivity. Front Syst Neurosci. 2010. 4: 19-
12. Hacker CD, Laumann TO, Szrama NP, Baldassarre A, Snyder AZ, Leuthardt EC. Resting state network estimation in individual subjects. Neuroimage. 2013. 82: 616-33
13. Hirsch J, Ruge MI, Kim KH, Correa DD, Victor JD, Relkin NR. An integrated functional magnetic resonance imaging procedure for preoperative mapping of cortical areas associated with tactile, motor, language, and visual functions. Neurosurgery. 2000. 47: 711-21
14. Jääskeläinen JRandell TWestphal MTonn JCRam ZLast accessed on 2013 Jun 20. Available from: http://www.springerlink.com/index/10.1007/978-3-7091-6090-9_6 .
15. Jack CR, Thompson RM, Butts RK, Sharbrough FW, Kelly PJ, Hanson DP. Sensory motor cortex: Correlation of presurgical mapping with functional MR imaging and invasive cortical mapping. Radiology. 1994. 190: 85-92
16. Kim SS, McCutcheon IE, Suki D, Weinberg JS, Sawaya R, Lang FF. Awake craniotomy for brain tumors near eloquent cortex: Correlation of intraoperative cortical mapping with neurological outcomes in 309 consecutive patients. Neurosurgery. 2009. 64: 836-45
17. Lanier WL. Brain tumor resection in the awake patient. Mayo Clin Proc. 2001. 76: 670-2
18. Lehéricy S, Duffau H, Cornu P, Capelle L, Pidoux B, Carpentier A. Correspondence between functional magnetic resonance imaging somatotopy and individual brain anatomy of the central region: Comparison with intraoperative stimulation in patients with brain tumors. J Neurosurg. 2000. 92: 589-98
19. Liu H, Buckner RL, Talukdar T, Tanaka N, Madsen JR, Stufflebeam SM. Task-free presurgical mapping using functional magnetic resonance imaging intrinsic activity. J Neurosurg. 2009. 111: 746-54
20. Manninen PH, Balki M, Lukitto K, Bernstein M. Patient satisfaction with awake craniotomy for tumor surgery: A comparison of remifentanil and fentanyl in conjunction with propofol. Anesth Analg. 2006. 102: 237-42
21. Meyer FB, Bates LM, Goerss SJ, Friedman JA, Windschitl WL, Duffy JR. Awake craniotomy for aggressive resection of primary gliomas located in eloquent brain. Mayo Clin Proc. 2001. 76: 677-87
22. Mitchell TJ, Hacker CD, Breshears JD, Szrama NP, Sharma M, Bundy DT. A novel data-driven approach to preoperative mapping of functional cortex using resting-state functional magnetic resonance imaging. Neurosurgery. 2013. 73: 969-82
23. Mogilner AY, Rezai AR. Epidural motor cortex stimulation with functional imaging guidance. Neurosurg Focus. 2001. 11: E4-
24. Mueller WM, Yetkin FZ, Hammeke TA, Morris GL, Swanson SJ, Reichert K. Functional magnetic resonance imaging mapping of the motor cortex in patients with cerebral tumors. Neurosurgery. 1996. 39: 515-20
25. Murphy K, Bodurka J, Bandettini PA. How long to scan.The relationship between fMRI temporal signal to noise ratio and necessary scan duration?. Neuroimage. 2007. 34: 565-74
26. O'shea JP, Whalen S, Branco DM, Petrovich NM, Knierim KE, Golby AJ. Integrated image- and function-guided surgery in eloquent cortex: A technique report. Int J Med Robot. 2006. 2: 75-83
27. Pereira LC, Oliveira KM, L’Abbate GL, Sugai R, Ferreira JA, da Motta LA. Outcome of fully awake craniotomy for lesions near the eloquent cortex: Analysis of a prospective surgical series of 79 supratentorial primary brain tumors with long follow-up. Acta Neurochir (Wien). 2009. 151: 1215-30
28. Sanai N, Berger MS. Glioma extent of resection and its impact on patient outcome. Neurosurgery. 2008. 62: 753-64
29. Sanai N, Polley MY, McDermott MW, Parsa AT, Berger MS. An extent of resection threshold for newly diagnosed glioblastomas: Clinical article. J Neurosurg. 2011. 115: 3-8
30. Santini B, Talacchi A, Casagrande F, Casartelli M, Savazzi S, Procaccio F. Eligibility criteria and psychological profiles in patient candidates for awake craniotomy: A pilot study. J Neurosurg Anesthesiol. 2012. 24: 209-16
31. Sarang A, Dinsmore J. Anaesthesia for awake craniotomy – Evolution of a technique that facilitates awake neurological testing. Br J Anaesth. 2003. 90: 161-5
32. See JJ, Lew TW, Kwek TK, Chin KJ, Wong MF, Liew QY. Anaesthetic management of awake craniotomy for tumour resection. Ann Acad Med Singapore. 2007. 36: 319-25
33. Serletis D, Bernstein M. Prospective study of awake craniotomy used routinely and nonselectively for supratentorial tumors. J Neurosurg. 2007. 107: 1-6
34. Shimony JS, Zhang D, Johnston JM, Fox MD, Roy A, Leuthardt EC. Resting-state spontaneous fluctuations in brain activity: A new paradigm for presurgical planning using fMRI. Acad Radiol. 2009. 16: 578-83
35. Shinoura N, Yamada R, Kodama T, Suzuki Y, Takahashi M, Yagi K. Preoperative fMRI, tractography and continuous task during awake surgery for maintenance of motor function following surgical resection of metastatic tumor spread to the primary motor area. Minim Invasive Neurosurg. 2005. 48: 85-90
36. Skucas AP, Artru AA. Anesthetic complications of awake craniotomies for epilepsy surgery. Anesth Analg. 2006. 102: 882-7
37. Stapleton SR, Kiriakopoulos E, Mikulis D, Drake JM, Hoffman HJ, Humphreys R. Combined utility of functional MRI, cortical mapping, and frameless stereotaxy in the resection of lesions in eloquent areas of brain in children. Pediatr Neurosurg. 1997. 26: 68-82
38. Szelényi A, Bello L, Duffau H, Fava E, Feigl GC, Galanda M. Intraoperative electrical stimulation in awake craniotomy: Methodological aspects of current practice. Neurosurg Focus. 2010. 28: E7-
39. Taylor MD, Bernstein M. Awake craniotomy with brain mapping as the routine surgical approach to treating patients with supratentorial intraaxial tumors: A prospective trial of 200 cases. J Neurosurg. 1999. 90: 35-41
40. Tieleman A, Deblaere K, Van Roost D, Van Damme O, Achten E. Preoperative fMRI in tumour surgery. Eur Radiol. 2009. 19: 2523-34
41. Tomczak RJ, Wunderlich AP, Wang Y, Braun V, Antoniadis G, Görich J. fMRI for preoperative neurosurgical mapping of motor cortex and language in a clinical setting. J Comput Assist Tomogr. 2000. 24: 927-34
42. Ulmer JL, Hacein-Bey L, Mathews VP, Mueller WM, DeYoe EA, Prost RW. Lesion-induced pseudo-dominance at functional magnetic resonance imaging: Implications for preoperative assessments. Neurosurgery. 2004. 55: 569-79
43. Ulmer JL, Krouwer HG, Mueller WM, Ugurel MS, Kocak M, Mark LP. Pseudo-reorganization of language cortical function at fMR imaging: A consequence of tumor-induced neurovascular uncoupling. AJNR Am J Neuroradiol. 2003. 24: 213-7
44. Zhang D, Johnston JM, Fox MD, Leuthardt EC, Grubb RL, Chicoine MR. Preoperative sensorimotor mapping in brain tumor patients using spontaneous fluctuations in neuronal activity imaged with functional magnetic resonance imaging: Initial experience. Neurosurgery. 2009. 65: 226-36