Intraoperative mapping and monitoring of the corticospinal tracts with neurophysiological assessment and 3-dimensional ultrasonography-based navigation

Clinical article

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Object

Preserving motor function is a major challenge in surgery for intraaxial brain tumors. Navigation systems are unreliable in predicting the location of the corticospinal tracts (CSTs) because of brain shift and the inability of current intraoperative systems to produce reliable diffusion tensor imaging data. The authors describe their experience with elaborate neurophysiological assessment and tractography-based navigation, corrected in real time by 3D intraoperative ultrasonography (IOUS) to identify motor pathways during subcortical tumor resection.

Methods

A retrospective analysis was conducted in 55 patients undergoing resection of tumors located within or in proximity to the CSTs at the authors' institution between November 2007 and June 2009. Corticospinal tract tractography was coregistered to surgical navigation-derived images in 42 patients. Direct cortical-stimulated motor evoked potentials (dcMEPs) and subcortical-stimulated MEPs (scrtMEPs) were recorded intraoperatively to assess function and estimate the distance from the CSTs. Intraoperative ultrasonography updated the navigation imaging and estimated resection proximity to the CSTs. Preoperative clinical motor function was compared with postoperative outcome at several time points and correlated with incidences of intraoperative dcMEP alarm and low scrtMEP values.

Results

The threshold level needed to elicit scrtMEPs was plotted against the distance to the CSTs based on diffusion tensor imaging tractography after brain shift compensation with 3D IOUS, generating a trend line that demonstrated a linear order between these variables, and a relationship of 0.97 mA for every 1 mm of brain tissue distance from the CSTs. Clinically, 39 (71%) of 55 patients had no postoperative deficits, and 9 of the remaining 16 improved to baseline function within 1 month. Seven patients had varying degrees of permanent motor deficits. Subcortical stimulation was applied in 45 of the procedures. The status of 32 patients did not deteriorate postoperatively (stable or improved motor status): 27 of them (84%) displayed minimum scrtMEP thresholds > 7 mA. Six patients who experienced postoperative deterioration quickly recovered (within 5 days) and displayed minimum scrtMEP thresholds > 6.8 mA. Five of the 7 patients who had late (> 5 days postoperatively) or no recovery had minimal scrtMEP thresholds < 3 mA. An scrtMEP threshold of 3 mA was found to be the cutoff point below which irreversible disruption of CST integrity may be anticipated (sensitivity 83%, specificity 95%).

Conclusions

Combining elaborate neurophysiological assessment, tractography-based neuronavigation, and updated IOUS images provided accurate localization of the CSTs and enabled the safe resection of tumors approximating these tracts. This is the first attempt to evaluate the distance from the CSTs using the threshold of subcortical monopolar stimulation with real-time IOUS for the correction of brain shift. The linear correlation between the distance to the CSTs and the threshold of subcortical stimulation producing a motor response provides an intraoperative technique to better preserve motor function.

Abbreviations used in this paper: CST = corticospinal tract; dcMEP = direct cortical-stimulated motor evoked potential; DT = diffusion tensor; FA = fractional anisotropy; IOUS = intraoperative ultrasonography; ROI = region of interest; scrtMEP = subcortical-stimulated MEP; SPGR = spoiled gradient echo; SSEP = somatosensory evoked potential.

Article Information

* Dr. Nossek and Mr. Korn contributed equally to this work.

Address correspondence to: Zvi Ram, M.D., Department of Neurosurgery, Tel Aviv Medical Center, 6 Weizman Street, Tel Aviv 64239, Israel. email: Zviram@tasmc.health.gov.il.

Please include this information when citing this paper: published online August 27, 2010; DOI: 10.3171/2010.8.JNS10639.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Upper: Cortical strip electrode and subcortical monopolar probe. Lower: Probe tip with tick marks at 1-mm intervals.

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    Calculated proximities with real-time US correction. Side-by-side comparison of preoperative MR image (left) and IOUS-based navigation image (right). Diffusion tensor imaging data is seen on the MR image and is manually translated to the analogous IOUS slice in offline analysis. A correction of 3 mm was made to the MR/DT imaging navigational coordinate. A scrtMEP threshold (Thresh) of 5.7 mA was correlated with this stimulation point. F = falx cerebri; prox = proximity; S = septum; SS = sagittal sinus; V = ventricle.

  • View in gallery

    Neuronavigation images (left) and corresponding scrtMEP traces (right). A: The stimulation point was > 20 mm from the CSTs (as depicted by DT imaging), and there was no positive scrtMEP to a maximum stimulation of 25 mA. B: The stimulation point was 8 mm from the CSTs, and the scrtMEP threshold was 4.0 mA. C: The stimulation point was approximately 1 mm from the CSTs, and the dcMEP threshold was 0.6 mA.

  • View in gallery

    Proximity correlation graph comprising 43 data points showing a near-linear relationship of the subcortical MEP threshold to the distance from the CST.

References

1

Bello LGambini ACastellano ACarrabba GAcerbi FFava E: Motor and language DTI Fiber Tracking combined with intraoperative subcortical mapping for surgical removal of gliomas. Neuroimage 39:3693822008

2

Berger M: Recent advances in neurosurgery. Curr Opin Oncol 2:6836901990

3

Berger MSOjemann GA: Intraoperative brain mapping techniques in neuro-oncology. Stereotact Funct Neurosurg 58:1531611992

4

Berger MSOjemann GALettich E: Neurophysiological monitoring during astrocytoma surgery. Neurosurg Clin N Am 1:65801990

5

Berman JIBerger MSChung SWNagarajan SSHenry RG: Accuracy of diffusion tensor magnetic resonance imaging tractography assessed using intraoperative subcortical stimulation mapping and magnetic source imaging. J Neurosurg 107:4884942007

6

Cedzich CTaniguchi MSchafer SSchramm J: Somatosensory evoked potential phase reversal and direct motor cortex stimulation during surgery in and around the central region. Neurosurgery 38:9629701996

7

Claus EBHorlacher AHsu LSchwartz RBDello-Iacono DTalos F: Survival rates in patients with low-grade glioma after intraoperative magnetic resonance image guidance. Cancer 103:122712332005

8

Duffau H: Intraoperative direct subcortical stimulation for identification of the internal capsule, combined with an image-guided stereotactic system during surgery for basal ganglia lesions. Surg Neurol 53:2502542000

9

Duffau HCapelle LDenvil DSichez NGatignol PTaillandier L: Usefulness of intraoperative electrical subcortical mapping during surgery for low-grade gliomas located within eloquent brain regions: functional results in a consecutive series of 103 patients. J Neurosurg 98:7647782003

10

Duffau HCapelle LSichez JFaillot TAbdennour LLaw-Koune JD: Intra-operative direct electrical stimulations of the central nervous system: the Salpetriere experience with 60 patients. Acta Neurochir (Wien) 141:115711671999

11

Ebeling USchmid UDYing HReulen HJ: Safe surgery of lesions near the motor cortex using intra-operative mapping techniques: a report on 50 patients. Acta Neurochir (Wien) 119:23281992

12

Fontaine DCapelle LDuffau H: Somatotopy of the supplementary motor area: evidence from correlation of the extent of surgical resection with the clinical patterns of deficit. Neurosurgery 50:2973032002

13

Kamada KTodo TOta TIno KMasutani YAoki S: The motor-evoked potential threshold evaluated by tractography and electrical stimulation. Clinical article. J Neurosurg 111:7857952009

14

Keles GELundin DALamborn KRChang EFOjemann GBerger MS: 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. J Neurosurg 100:3693752004

15

Kombos TSuess OCiklatekerlio OBrock M: Monitoring of intraoperative motor evoked potentials to increase the safety of surgery in and around the motor cortex. J Neurosurg 95:6086142001

16

Kombos TSuess OFunk TKern BCBrock M: Intra-operative mapping of the motor cortex during surgery in and around the motor cortex. Acta Neurochir (Wien) 142:2632682000

17

Mikuni NOkada TEnatsu RMiki YHanakawa TUrayama S: Clinical impact of integrated functional neuronavigation and subcortical electrical stimulation to preserve motor function during resection of brain tumors. J Neurosurg 106:5935982007

18

Mikuni NOkada TNishida NTaki JEnatsu RIkeda A: Comparison between motor evoked potential recording and fiber tracking for estimating pyramidal tracts near brain tumors. J Neurosurg 106:1281332007

19

Mori SCrain BJChacko VPvan Zijl PC: Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann Neurol 45:2652691999

20

Ozawa NMuragaki YNakamura RHori TIseki H: Shift of the pyramidal tract during resection of the intraaxial brain tumors estimated by intraoperative diffusion-weighted imaging. Neurol Med Chir (Tokyo) 49:51562009

21

Ozawa NMuragaki YNakamura RIseki H: Identification of the pyramidal tract by neuronavigation based on intraoperative diffusion-weighted imaging combined with subcortical stimulation. Stereotact Funct Neurosurg 87:18242009

22

Ozawa NMuragaki YNakamura RLseki H: Intraoperative diffusion-weighted imaging for visualization of the pyramidal tracts. Part II: clinical study of usefulness and efficacy. Minim Invasive Neurosurg 51:67712008

23

Qazi AARadmanesh AO'Donnell LKindlmann GPeled SWhalen S: Resolving crossings in the corticospinal tract by two-tensor streamline tractography: Method and clinical assessment using fMRI. Neuroimage 47:Suppl 2T98T1062009

24

Sanai NBerger MS: Intraoperative stimulation techniques for functional pathway preservation and glioma resection. Neurosurg Focus 28:2E12010

25

Smith JSChang EFLamborn KRChang SMPrados MDCha S: Role of extent of resection in the long-term outcome of low-grade hemispheric gliomas. J Clin Oncol 26:133813452008

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