ORIGINAL ARTICLE

Intraoperative DTI and brain mapping for surgeryof neoplasm of the motor cortex and the corticospinal tract:our protocol and series in BrainSUITE

Giancarlo D’Andrea & Albina Angelini &Andrea Romano & Antonio Di Lauro & Giovanni Sessa &

Alessandro Bozzao & Luigi Ferrante

Received: 29 March 2011 /Revised: 19 September 2011 /Accepted: 25 September 2011 /Published online: 28 February 2012# Springer-Verlag 2012

Abstract We report our preliminary series of patients trea-ted for lesions involving the motor cortex and the cortico-spinal tract in BrainSuite, with intraoperative MRI,tractography and “neuronavigated” electrophysiologicalcortical and subcortical mapping. An exact localization ofthe cortical and subcortical functional areas is mandatory forexecuting surgery of intra-parenchymal neoplasm involvingthe motor cortex and the corticospinal tract. Nowadaysmodern technology offers a variety of tools to reduce asmuch as possible postoperative deficits during surgery ofcerebral eloquent areas. From December 2008 and June2010, 18 patients underwent functional surgery, for neo-plasm involving the motor cortex and/or the subcorticalpathway, in BrainSuite. Our preliminary series include 14gliomas and 4 metastases; Table 1 summarizes all of thedata. We included in this series patients with completeremoval of lesions of eloquent areas with an average dis-tance from the corticospinal tract of 4 mm. Six neoplasmswere considered in contact and/or involving the motor cor-tex, while in 18 cases (100%) the tumour involved eloquent

areas concerning the corticospinal tract. All of the patientsunderwent complete removal of the lesion as subsequentlydemonstrated by intraoperative postsurgical MRI. Our serieshighlights the good integration and the high compatibilitybetween BrainSUITE with 1.5 T intraoperative magneticfield and neurophysiological monitoring. We strongly be-lieve that intraoperative MRI with DTI allows us to treatcomplex surgery tumours that without its auxilium wewould not be able to deal with.

Keywords Intraoperative MRI . Brain mapping .

Corticospinal tract . Motor cortex

Introduction

An exact localization of the cortical and subcortical func-tional areas is mandatory for executing surgery of intra-parenchymal neoplasm of the cerebral motor cortex. It iscurrently believed that the main goals of this surgery are tomaximize the excision and to minimize the operative riskand the postoperative morbidity.

Modern technology offers a number of tools to reduce asmuch as possible postoperative deficits during surgery ofcerebral eloquent areas. Perirolandic gyri have been tradi-tionally identified by neurophysiologic monitoring of thephase reversal and by the direct motor cortex stimulation.fMRI and neuronavigation define the “functional neurona-vigation” and are capable of improving the definition ofeloquent areas by the comparison of the previously detectedfunctional areas (fMRI) and the brain mapping recordings.

Preoperative MRI is a good but insufficient tool for intra-operative “functional” neuronavigation on lesions within orclose to eloquent areas because it presents a high possibility of

G. D’Andrea (*) :A. Angelini :G. Sessa : L. FerranteS Andrea Hospital, Institute of Neurosurgery,University of Rome “La Sapienza”,V. Raineri 27,00151 Rome, Italye-mail: gdandrea2002@yahoo.it

A. Romano :A. BozzaoS Andrea Hospital, Institute of Neuroradiology,University of Rome “La Sapienza”,Rome, Italy

A. Di LauroS Andrea Hospital, Institute of Anesthesiology,University of Rome “La Sapienza”,Rome, Italy

Neurosurg Rev (2012) 35:401–412DOI 10.1007/s10143-012-0373-6

inaccuracy due to the brain shift. Intraoperative DTI andtractography guarantee the update of anatomical data so thatthe neurosurgeon can exactly localize the corticospinal tractwithin the white matter, reducing the risk of injuring it. Intra-operative MRI is fundamental to correct the main factor ofinexactitude proper of usual neuronavigation, only based onpreoperative imaging; that is the brain shift. We report ourpreliminary series of patients treated for lesions involving themotor cortex and the corticospinal tract in BrainSuite withintraoperative MRI, tractography and “neuronavigated” elec-trophysiological cortical and subcortical mapping.

Methods

Surgical series

From December 2008 and June 2010, 18 patients underwentfunctional surgery in BrainSuite for neoplasm involving themotor cortex and/or the subcortical pathway. Our prelimi-nary series include 11 high-grade gliomas, 2 low-gradegliomas, 1 oligodendroglioma and 4 metastases; Table 1summarizes all of the data.

All the patients were evaluated at different stages: at ad-mission, after surgery, at discharge and 1 month after theprocedure. Clinical assessment was performed by the sameneurosurgeon (GS) not involved in the surgery of these cases,and the follow-up was reported and classified as worsened,unchanged or improved 6 months after the surgery.

We operated 18 cases, 9 females and 9 males with anaverage age of 56.05 years; 2 cases were low-grade gliomas,1 oligodendroglioma, 4 metastases and 11 high-grade glio-mas. All the cases involved tumour of eloquent areas affect-ing the motor cortex and/or the pyramidal tract; in 18 cases(100%), the tumour concerned the white matter tract, whilein 6 (33.3%) the motor cortex. We included in this seriespatients with complete removal of lesions of eloquent areaswith an average distance from the corticospinal tract of4 mm (Table 1).

All the patients with a preoperative severe or permanentdeficit, with an incomplete resection and without a completepreoperative and intraoperative study, were excluded. Thecomplete dataset has been subdivided into 3 subgroupsrelating to the histology; all the subgroups were comparedon the basis of their results, behavior and outcome (Table 2).

Preoperative MR protocol

Preoperative study was performed with a 1.5-T magnet (Mag-netom Sonata, Siemens, Erlangen, Germany), twin to the onepresent in the operating room. The following sequences wereacquired: T2, FLAIR, isotropic volumetric T1-weightedmagnetisation-prepared rapid acquisition gradient echo beforeand after intravenous administration of paramagnetic contrastmaterial and diffusion tensor sequences.

The DTI study was carried out through 12 non-collineardirections (b value00 and 1,000 s/mm2) with echo-planarsequences (TE/TR092/9,400 ms, matrix0128×128, FOV0

Table 1 Summary of intraoperative data

Case Name Age Sex Histology Surgical risk Resection Distancefrom tract

Distance ofMEP (mm)

Immediateoutcome

Qualityof life

Recovery

1 A. M. 68 M Low grade Tract Complete In contact 0 Improved Excellent Immediate

2 B. S. 39 F Metastasis Tract Complete 7 mm 7 Unchanged Excellent Immediate

3 C. M. 77 M Glioma Tract Complete In contact 0 Improved Excellent Immediate

4 D. C. 67 M Glioma Tract Complete In contact 0 Unchanged Excellent Immediate

5 D. M. N. 42 M Metastasis Tract/cortex Complete In contact 5 Improved Excellent Immediate

6 F. V. 66 F Glioma Tract Complete 15 mm 15 Unchanged Excellent Immediate

7 P. A. 37 M Oligodendroglioma Tract/cortex Complete In contact 2 Mild paresis Excellent 3 months

8 S. M. 65 F Low grade Tract/cortex Complete In contact 0 Unchanged Excellent Immediate

9 M. L. 66 F Glioma Tract Complete 4 mm 4 Improved Excellent Immediate

10 R. G. 40 F Glioma Tract Complete 12 mm 12 Improved Excellent Immediate

11 Q. A. 26 M Glioma Tract Complete 6 mm 6 Improved Excellent Immediate

12 A. G. 68 F Glioma Tract Complete 8 mm 8 Improved Excellent Immediate

13 P. C. 50 F Glioma Tract Complete In contact 2 Improved Excellent Immediate

14 P. I. 50 M Metastasis Tract/cortex Complete In contact 0 Unchanged Excellent Immediate

15 C. A. 75 F Glioma Tract Complete In contact 2 Improved Optimum Immediate

16 C. L. 76 M Glioma Tract Complete In contact 0 Unchanged Optimum Immediate

17 R. A. 54 F Glioma Tract/cortex Complete In contact 0 Improved Excellent Immediate

18 D. N. 43 M Metastasis Tract/cortex Complete In contact 0 Monoparesis Excellent 1 month

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230 mm, slice thickness01.9 mm, bandwidth01502 Hz/Px,slices060, no gap, acquisition time06.18 min, 3 NEX). Thetractography processing was carried out by a planning soft-ware iPlan 2.6 (BrainLAB AG, Feldkichen, Germany) witha method similar to the one presented by Basser et al., Moriet al. and Stieltjes et al. [3, 41, 70].

Colour maps were employed to define an appropriateregion of interest (ROI) for the following tractographicprocedure. The fibre tracking technique contemplates the3D reconstruction of white matter trajectories of CST byemploying a fractional anisotropy threshold of 0.17 and aprocessing angle above 55°. The posterior arm of the inter-nal capsule and precentral gyrus identified by functionalMRI for the pyramidal tract were chosen as the site of thepositioning of the ROIs (always using the same size of ROI,50 pixels). Tracking was initiated in both the retrograde andorthograde directions according to the direction of the prin-cipal eigenvector in each voxel of the region of interest.Mean data processing time of the CST was 2–3 min.

The acquired trajectories were transformed into tri-dimensional objects. Compared with the previously recon-structed trajectories, the outer margins of these objects wereautomatically enlarged by the software by 2 mm in everydirection. Dilating the 3D reconstructed trajectories allowed

registration errors to be minimized (usually below 3 mm)and a safer margin for surgery to be introduced. Tracto-graphic processing was performed by the same operator(RA). The trajectories were considered suitable for the sur-gical planning in case of no interruptions on any of thelayers at the level of the lesion.

All tractography results were saved in a file that includedx/y/z coordinates for each tract, and then this data wasimported (together with b00 diffusion images) into thenavigation software (iPlan 2.6, BrainLAB AG, Feldkichen,Germany). After rigid registration of b00 images with avolumetric anatomical dataset and after ensuring data con-sistency (discrepancies ≤3 mm) in the tumour area, trajec-tory reconstructions can be visualized within anatomicalimages. The margins of the fibres are then segmented topermit their definition as “objects” within the neuronaviga-tion system and their visualisation during surgery. Thisprocessing is usually performed the day before the proce-dure and takes approximately half an hour. The overall timefor this data processing, which was generally performed theday prior to surgery, had an average duration of 30 min.

Preoperative study was completed with functional MRIperformed following the movements our neurophysiologist(AA) suggested to the patients. We usually reviewed the

Table 2 Analysis of four subgroups relating to their histology

Case Age Histology Surgical risk Resection Distance from tract Distance of mep Immediate outcome Recovery

Group 1

3 77 Glioma Tract Complete In contact 0 mm Improved Immediate

4 67 Glioma Tract Complete In contact 0 mm Unchanged Immediate

6 66 Glioma Tract Complete 15 mm 15 mm Unchanged Immediate

9 66 Glioma Tract Complete 4 mm 4 mm Improved Immediate

10 40 Glioma Tract Complete 12 mm 12 mm Improved Immediate

11 26 Glioma Tract Complete 6 mm 6 mm Improved Immediate

12 68 Glioma Tract Complete 8 mm 8 mm Improved Immediate

13 50 Glioma Tract Complete In contact 2 mm Improved Immediate

15 75 Glioma Tract Complete In contact 2 mm Improved Immediate

16 76 Glioma Tract Complete In contact 0 mm Unchanged Immediate

17 54 Glioma Tract Complete In contact 0 mm Improved Immediate

Average 60.45 4.09 mm 4.45 mm 100%

Group 2

1 68 Low grade Tract Complete In contact 0 mm Improved Immediate

7 37 Oligodendroglioma Tract/cortex Complete In contact 2 mm Mild paresis 3 months

8 65 Low grade Tract/cortex Complete In contact 0 mm Unchanged Immediate

Average 56.6 in contact 0.6 mm 66.60%

Group 3

2 39 Metastasis Tract Complete 7 mm 7 mm Unchanged Immediate

5 42 Metastasis Tract/cortex Complete In contact 5 mm improved Immediate

14 50 Metastasis Tract/cortex Complete In contact 0 mm Unchanged Immediate

18 43 Metastasis Tract/cortex Complete In contact 0 mm Monoparesis 1 month

Average 43.5 1.75 mm 3 mm 75%

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following muscles: the orbicularis oris, the orbicularis ocu-lis, the biceps, the deltoid, the common extensor of fingers,the abductor of the thumb, the abductor of the fifth finger,the quadriceps, the anterior tibialis, allux long extensor andallux long flexor.

Intraoperative MR imaging

Usually we do not perform intraoperative presurgical MRIfor start intervention because of infrared matching of head’spatients with previous acquired volumetric exams; but forprone position. In the first cases, we performed it acquiringvolumetric isometric T1-weighted images and DTI with thesame characteristics as those previously obtained withoutparamagnetic contrast material administration for subse-quent fusion and navigation.

These exams allows an automatic fusion with the previ-ous acquired data because of a multichannel coil containingstereotactic markers that are “read” by the neuro-navigatorcamera and then registered by the neuro-navigator itself.The same specific BrainLab software of preoperative examis utilized to build the new tractography, successively com-pared with the previous processed tractography. The averageof the total acquisition time was less than 10 min because ofthe simplified MR data registration.

Moreover, in this kind of surgery, we perform the firstintraoperative MRI after the dural opening acquiring anintraoperative volumetric MRI for navigation and an intra-operative DTI for tractography. This step is fundamental tocorrect the possible brain shift due to gravity’s effect on thebrain related to surgical position, surgical retraction of brain,edema, drainage of CSF after dural opening, administrationof osmotic diuretics and mass effect of the tumour (Figs. 1and 2). Total acquisition and processing time average was

about 15 min. We routinely perform a volumetric MRI and anew DTI with tractography after dural opening to correct thebrain shift.

In all of the cases involving the motor cortex, we per-formed a “neuronavigated” brain mapping following thedata of preoperative functional MRI to localize the previ-ously elicited areas (Figs. 7 and 8). The functional areaswere investigated after brain shift correction by corticalbrain mapping and indicated.

After this step the surgeon proceeded with the removal.When the neurosurgeon was confident that most of thelesion was removed, and before approaching the mass closeto the white matter tract, intraoperative MRI was againperformed to show the residual lesion and to correct theeventual brain shift.

The same neuroradiologist reconstructed the CST and thenew tractographic objects were uploaded in the neuro-navigation system and subsequently used for further surgeryand for intraoperative subcortical stimulation. At the end ofthe procedure, we performed the last MRI to check thecomplete removal and the sparing of the corticospinal tract.

Intraoperative electrical mapping

We track the mono or bipolar probe for neuronavigationthrough a reference star that is recognized and “neuro-nav-igated”, therefore using it for the dual role of pointer andelectrical probe (Fig. 3). Motor evoked potentials wererecorded with subdermal platinum/iridium needle electrodes(MRI compatible), positioned on muscles of limbs and face.Selected muscles are the same elicitated during preoperativefunctional MRI.

Our neurophysiologist (AA) prepared the patients somedays before the functional MRI to correctly perform therequested movements. All patients underwent total generalintravenous anesthesia with propofol and remifentanyl withcontinuous infusion at a constant dose of, respectively,6 mg/kg/h and 0.05 mg/kg/min, allowing the reading ofneurophysiological data without interference.

In all the cases, evaluation of the motor area was con-firmed by the study of the phase reversal (Figs. 4, 5 and 6)and with “neuronavigated” brain mapping. The stimulationof a peripheral nerve was used to confirm the train offour muscular contractions; to identify the central sulcus,N20-P25 and P37-N45 phase reversal of somatosensoryevoked potential were recorded, using cortical stripelectrodes.

For the electrophysiological monitoring of motor func-tion of the CST, first pre-central cortex was stimulated inorder to identify a positive control of motor evoked poten-tials. Later on we also stimulated subcortical fibers. Theintensity of cortical stimulation was increased by 1 to5 mA up to a maximum of 15 mA for cortical MEPs and

Fig. 1 Intraoperative tractography has been compared with the preop-erative exam clearly demonstrating an important shift of the whitematter bundles in all of the three planes

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by 1 mA to a maximum of 3 mA for subcortical MEPs.Frequency given as 60 Hz pulse duration 2–3 ms.

Electromyograms were measured at the thenar mus-cle, orbicularis muscle, the quadriceps femoris muscle,the anterior tibial muscle, deltoid muscle, extensor dig-itorum, thumb extensor muscle, short flexor of the bigtoe muscle and the gastrocnemius muscle on both sides.

Results

Volumetric preoperative and functional MRI demonstrated18 intraparenchymal neoplasms. All the patients underwentcomplete removal of the lesion as subsequently demonstrat-ed by intraoperative postsurgical MRI.

Histological exam revealed 2 low-grade gliomas, 1 oligo-dendroglioma, 4 metastases and 11 high-grade gliomas. High-grade gliomas were included in group 1, low-grade gliomas

and the oligodendroglioma in group 2 and metastases in group3. In 10 cases of group 1 (90,9%), the tumour involved theeloquent areas concerning the corticospinal tract, while onlyin case 17 was the lesion considered in contact and/or involv-ing the motor cortex. In groups 2 and 3, we noted a differentpattern with 3/4 of cases (75%) and 2/3 of cases (66.6%),respectively in contact and/or involving the motor cortex. Theoverall data illustrated 6 cases in contact and/or involving themotor cortex; while in 18 cases (100%), the tumour involvedeloquent areas concerning the corticospinal tract.

The motor function has been preserved in all patients ofgroup 1. In this respect, two patients (case 7—group 2 andcase 18—group 3) showed, respectively, transient weaknessof the left side which dramatically improved 1 month laterand then disappeared after 3 months; while mild paresis ofleft hand improved after only 1 month. In both cases, thelesions were considered in contact with the motor cortex andthe corticospinal tract. The distance between the lesions and

Fig. 2 3D reconstruction againcomparing preoperative andintraoperative tractographyafter extracranial shift of thelesion

Fig. 3 We track the mono or bipolar probe for neuronavigationthrough a reference star that is recognized and “neuro-navigated” sousing it for the dual role of pointer and electrical stimulation Fig. 4 Intraoperative phase reversal

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the tract was considered 0 and the subcortical “neuronavi-gated” MEPs were performed, respectively, at 2 mm and incontact with the tract. The tumours were completely re-moved and the patients rapidly improved, presenting anexcellent quality of life at discharge; the patient no. 7 wenteven back to his work as cooker after 3 months.

Cortical MEPs following preoperative functional MRIand after brain shift correction were performed also in cases5, 7, 8, 14, 18 (group 2 and 3) and 17 (group 1) with thesame methods to choose the optimal site for corticectomyand brain retraction. The white matter bundle containing thepyramidal tract was visualized in all patients in pre- andintraoperative MRI (Fig. 7).

During surgery, close to the pyramidal tract, several elec-trical “neuronavigated” stimulations were repeatedly per-formed following the neuronavigation after intraoperativevolumetric MRI and DTI, demonstrating the deep residualand correcting the eventual brain shift (Figs. 8 and 9). Theoverall average distance (groups 1–3) on preoperative tractog-raphy between the lesion and the corticospinal tract was2.26 mm and the average distance between the corticospinaltract and the site of subcortical MEP was 3.5 mm. In partic-ular, the average distances were 4.09 and 4 45 mm in group 1,0 and 0.6 mm in group 2 and 1.75 and 3 mm in group 3,respectively, on preoperative and intraoperative data images.

In cases 6 and 10, the distances of the lesion from thecorticospinal tract both in preoperative evaluation and insubcortical MEPs were 15 and 12 mm; in those cases, the

tract was considered sufficiently far from the lesion for asafe and complete removal. These cases dramatically affectthe average measured distances relating to groups 2 and 3showing a closer relationship with corticospinal tract but 6/11 (54.5%) of cases of group 1 were in contact with it. Incases 2, 11 and 12, the distance of CST from lesion was,respectively, 7, 6 and 8 mm. The remaining 13 cases (72%)were judged in contact with the corticospinal tract (12 casescontacting it and case 9 at 4 mm).

Therefore, summing up, we performed subcortical MEPsin 11/18 cases (61%) between 0 and 2 mm from cortico-spinal tract, in 6/18 (33%) between 4 and 8 mm and in 2/18cases between 12 and 15 mm. We detected the corticospinaltract in all the cases, exception made for cases 6 and 10 inwhich it was far from the lesion.

During our process we always assumed that the neuro-navigation system had an average error of 0.79±0.25 mmand a maximum error of 2.0 mm. Intraoperative postsurgicalMRI demonstrated a complete removal in all the cases ofthis series (100%) and the postoperative outcome was ex-cellent in all the patients. Immediate postoperative outcomewas again optimum even if patient no. 7 complained of amild weakness of the left arm that rapidly improved beforethe discharge. The patient recovered in 3 months going backto his usual work. Quality of life at discharge and during thefollowing controls at 6 months was excellent and all thepatients came back to their private life and work. Theimmediate postoperative overall outcome was excellent in89% of the cases and we registered a transient worsenedmotor deficit only in 2 cases (11%).

Discussion

In malignant neoplasm, survival can improve with aggres-sive and complete tumour resection [1, 5, 12, 31, 64], but itmust be carefully taken into consideration postoperativequality of life and possible functional deficits. Quality oflife of patients affected by malignant neoplasm in eloquentareas must be a priority parameter [19] to choose surgeryrather than biopsy because of their expected short survival.Moreover excellent quality of life and no postoperativedeficits must be pursued also in surgery of benign neoplasmaffecting the motor cortex. This goal can be achievedthrough the exact localization and consequent preservationof the cortical and subcortical functional areas.

Although maximal excision of glioma appears to bethe first tool to influence the natural history of thistumour [18], many series report unacceptable rates(13–27.5%) of severe and permanent postoperative def-icits [7, 10, 65, 77]. In current opinion, maximizing [1,21, 22, 38, 39, 42, 63] the excision and minimizing theoperative risk and the postoperative morbidity [22, 56,

Fig. 5 Intraoperative phase reversal—surgical field

Fig. 6 Intraoperative localization of motor cortex

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57, 72, 75] are the main goals of this surgery [18, 23,28, 53, 69, 71, 76]; and intraoperative neurophysiolog-ical tools are indispensable for it [74].

Our operative protocol to achieve these results includes:

1) Neuronavigated brain mapping with fMRI and directcortical stimulation for surgery of lesions involving themotor cortex.

2) Intraoperative MRI with DTI update for reconstructionof pyramidal tract after dural opening and during CSTapproaching in tumour debulking with subcortical “neu-ronavigated” CST stimulation.

Neuronavigated brain mapping with fMRI and directcortical stimulation

The identification of the motor cortex is the first step in thissurgery and must be completed before starting the removalof lesion affecting the motor cortex, or also superficiallesions near to it. Perirolandic gyri have been traditionallyidentified by neurophysiologic monitoring of the phase re-versal and by the direct motor cortex stimulation [51, 54],but Romstock et al. [60] report many papers demonstratinglimitations and failure of this techniques especially for peri-rolandic mass lesions.

Fig. 7 “Neuronavigated” brainmapping following the dataof preoperative functional MRIto localize the previouslyelicited areas

Fig. 8 “Neuronavigated” brainmapping following the dataof preoperative functional MRIto localize the previouslyelicited areas—surgical field

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Suess et al. [74] reported 48 cases where the stimulation siteswere visualized using the neuronavigation and stated that thisprocedure helped to better identify the stimulation sites and theprecentral gyrus. The success rate of phase reversal identifica-tion of the motor cortex ranges between 82% and 97% [18, 60,74] with 10% to 18% of questionable or impossible localizationbecause the presence of a tumour produces a high variability ofSEP latencies and amplitudes. Duffau [19] observes that phasereversal gives informations about the site of central sulcus butdoes not allow the surgeon to know “direct information of theorganization of retro- and precentral cortices”.

Electrophysiological difficulties must also be taken intoconsideration because the tumour can desynchronize theafferent electrical impulses, the mass effect distorts thecortical electrical dipoles on the brain surface and the sur-geon could not choose the appropriate site of recording [66].Literature reports that brain mapping alone allows identifi-cation of the primary motor cortex in only 60% of cases [35]but a high success rate of cortical stimulation of 97% and91% has been reported respectively in Cedzich’s (58 cases)[10] and in Suess’s series (255 cases) [74].

Some authors [6, 22, 30, 67] stated that the combinationof neurophysiological monitoring and functional MRI(fMRI) improves the accuracy of localization of the motorcortex [2, 6, 20, 25, 33, 40, 67, 73] and many papers [9, 37,61, 62, 78] outline a high concordance between functionalMRI and direct cortical stimulation. Agreeing with theirresults, we found a high concordance between functionalMRI and intraoperative brain mapping; plus we also agreewith Bello et al. [4] that suggested a strong connection alsobetween DTI and subcortical mapping.

In our opinion, the combination of fMRI and direct corticalstimulation improves the sensitivity of each technique

reducing pitfalls (BOLD effect, motion-related artifacts byheartbeat, breathing or head motion and a too sensitive signalto large draining veins with a poor spatial resolution for fMRI[11, 76] and electrical artifacts for direct cortical stimulation)and also defining the “functional neuronavigation” [45, 46,50]; increasing the definition of eloquent areas by the com-parison of the previously detected functional areas (fMRI) andthe brain mapping recordings too. Therefore the combi-nation of these techniques reduces time of surgery andobviously the “neuronavigated cortical stimulation” ispossible because of the possibility of tracking the stim-ulation probe in neuronavigation system through a ref-erence star. Such protocol is clearly mandatory when acorticectomy or a gyral dissection is required in surgeryof intraparenchymal lesions.

Intraoperative MRI and tractography with neuronavigatedsubcortical CST stimulation

In order to improve GTR resection of tumours near the CST,our goal has been removal between 0 and 5 mm from thecorticospinal tract indentified after MRI intraoperativeupdating. Many authors consider the resection close toCST risky and preferred to maintain a “safe distance” fromwhite bundles in order to reduce the postoperative transient/permanent morbidity.

Gonzalez-Darder et al. [22] observed an increase of ex-tent of tumour resection followed by an increased rate ofproduced neurological deficits when tractography is theroute into navigator; the authors [22] perform subcorticalstimulations at the average distance of 7.3±3.1 mm follow-ing the neuronavigator with preoperative tractographic datadefining a safe distance of 8–10 mm and reporting a rate of

Fig. 9 “Neuronavigated”subcortical mapping

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70% of immediate postoperative deficits, reduced to 47%one month after using.

Carrabba et al. [8] planned not to resect white matterfurther than 8 mm from corticospinal tract, reporting a highrate of immediate postoperative deficits (59%) when thecorticospinal tract was identified by subcortical stimulationand a 10% rate when it was not detected, resulting in 6.5%and 3.5%, respectively of permanent deficits.

Kamada et al. [30] report a surgical strategy with subcor-tical stimulation and DTI integrated into navigation quitesimilar to our method, driving their resection up to 5 mmfrom the corticospinal tract; but again the loss of intraoper-ative update can play a considerable role.

Keles et al. [32] stated that intraoperative subcortical iden-tification of corticospinal tract is more prone to develop tran-sient (27%) or permant (13%) deficits. In fact he reports [32]7.6% of permanent postoperative deficits after demonstrating,by subcortical stimulation, a lesion located within or adjacentthe corticospinal tract and stating that this risk decreases to2.3% when the subcortical stimulation is negative. Yu et al.[79] report an extent of resection up to 5 mm from the tract.These data disagree with our findings probably because wealso have the opportunity to update DTI data when we arequite close to the tract, which changes the situation.

Many authors [32, 43, 47] clearly assert an importantshifting of the deep tumour portions during resection andconsequently of the white matter tracts. It has been de-scribed that preoperative MRI and DTI reconstruction anddata planning can be inaccurate [53] because of brain shift,surgical retraction, mass effect, gravity related to surgicalposition, extension of the excision, drainage of CSF, edemaand intraoperative osmotic diuretics administration [14, 24,26, 44, 48, 55, 58].

It is necessary to consider standard neuronavigation,without intraoperative upgrade [43, 44, 49], inaccurate[53] for this kind of surgery because of brain shift andbecause preoperative MRI is a good but insufficient toolfor intraoperative “functional” neuronavigation.

In our protocol preoperative MRI is always corrected bymultiple intraoperative MRI after dural opening and whenwe approach CST after a near total resection, we acquire anintraoperative volumetric MRI fusing it with preoperativedata and planning for precise navigation and an intraoper-ative DTI for tractography to approach residual tumour inproximity of CST and to improve reliability of MEP bydirect subcortical stimulation.

We believe this acquisition is mandatory because brainshift affects not only the position of superficial brain areasbut also the one of the deep white matter. Although preop-erative reconstruction of corticospinal tract allows the neu-rosurgeon to prevent postoperative neurological deficits [13,27], this elaboration has some pitfalls (signal of poor spatialresolution, close dependence from the operator during fibre

tracking) but the biggest limitation for accuracy and reliabil-ity is still the brain shift [50, 52, 79].

Brain shift is a serious problem in this type of surgery:even after a simple craniotomy has been described up to0.5–1 cm [16, 23] and once the dura was opened too [16,29]. In our experience, we registered a shift of the whitematter bundles simply after dural opening up to 14 mm andNimsky reported a shift up to 20–24 mm [26, 47, 48]. Thisshifting is magnified during tumour debulking and is unac-ceptable when we approach the CST with the neoplasm atdirect contact with it.

Despite intraoperative tractography is a reliable tool forsafe surgery near the CST, there are some pitfalls to consider:(1) tractography did not identify all fibres of pyramidal tractfor crossing fibre effect, (2) fibre tracking does not accuratelyestimate the size of the fibre bundle in pathologic conditions(peritumoural edema influenced the anisotropy of water mol-ecules) and (3) fibre tracking algorithms differ in their expres-sion of three-dimensional tracts. For these reasons, weadvocate the neurophysiologic “neuronavigated” monitoringfor compensation of these drawbacks. Subcortical MEPs com-plete intraoperative functional data [6, 15, 30, 34] and betterdefine the boundaries of corticospinal pathway and, duringsurgery, can be repeated more and more to identify the areawhere the corticospinal tract runs.

Even if Duffau et al. [17] stated that direct fibre stimula-tion is safe, accurate and reliable, Kamada et al. [30] observesome technical difficulties, such as selection of optimalstimulus point, visually indistinguishable subcortical path-ways, continuously interrupted surgery and long wastedtime.

Again, the integration of the neurophysiological techni-ques with the neuronavigation system, especially based onthe intraoperatively reconstructed CST objects [59], im-prove the precision of stimulation and reduce the time ofthe surgical procedure. We absolutely agree with Gonzalez-Darder et al. [22] when reporting a reduced time of identi-fication and of electrical stimulation of corticospinal tract byusing neuronavigation.

For what we are aware of, only another paper reports theuse of intraoperative tractography integrated with subcorti-cal CST MEP monitoring for the surgery in Motor Area[36]. According to the author [36], we report an optimalfunctional outcome with a higher rate of complete excisionand approximation to the pyramidal tract. In particular wereach a verified average distance between the corticospinaltract and the site of subcortical MEP of 3.93 mm.

Duffau [18] observes that intraoperative electrical stimula-tion, despite possible transient immediate postoperative defi-cits, improves results of gliomas surgery extending theindications to lesions being considered inoperable. He [18]reports a 95% of normal neurological outcome after surgery ofeloquent areas within 3 months even with some improvement

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and decrease of seizure in 80% of cases. Similarly to ourexperience Nimsky et al. [46] reported mild postoperativedeficits completely recovered during prolonged postoperativecourse and only 1 case of motor deficit after 3 months.

In literature we found, similarly to our series, a rapidresolution after immediate postoperative deficits [4, 8, 18,22, 68, 74]. We do think that the higher incidence of post-operative deficits that other authors report when they per-formed CST stimulation, although this should be due tosurgical traction, heat from bipolar coagulation, cytotoxicedema and/or microvascular reorganization [22], is causedby not updated and not reliable information regarding thespatial (DTI tractography) and functional (subcortical elec-tric stimulation) anatomy of the CST.

We believe the gold standard for this surgery is a com-bined and integrated approach of a multidisciplinary team ofneurosurgeon, neuroradiologist and neurophysiologist. Inparticular, the intraoperative update of anatomic and func-tional data, allows to reverse the surgical strategy: the use ofa stimulator probe “neuronavigated” onto updated tracto-graphic objects (CST reconstructed) guarantees the controlof the integrity of the tract before the removal of the residualvolume of the lesion, instead of verifying the integrity of thetract after his injury. The goal is not to remove and to checkbut to verify after an intraoperative-guided removal.

Conclusion

Surgery on lesions involving the motor cortex and thecorticospinal tract must maximize the resection respectingthe functionality of these eloquent areas. Postoperative qual-ity of life must be a crucial parameter in patients affected bymalignant neoplasms with short survival period. Our seriesconfirms the good integration and the compatibility betweenBrainSUITE with 1.5 T intraoperative magnetic field andneurophysiological monitoring. The few cases we reportindicate a good correspondence between MRI and brainmapping and demonstrate that in this kind of surgery amultidisciplinary approach is mandatory with fMRI, preop-erative and intraoperative DTI and brain mapping.

Acknowledgements Special thanks to Doctor Filippo Scotto for hisirreplaceable, careful and immediate technical support.

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Comments

Christopher Nimsky, Marburg, GermanyThe authors report on a series of patients with lesions close to the

motor system that were operated on with intraoperative MRI guidance,tractography, as well as brain mapping. This paper nicely demonstrateshow all these techniques can be combined in one setting and how thedifferent methods may contribute to the goal of maximum resectionwhile preserving neurological function. In the surgery of such lesions,there are two opposing strategies: there are groups operating suchlesions awake and on the other hand, there are groups relying onlyon preoperative functional and structural data.

Probably a sensitive combination of both extremes will be theoptimal strategy. Further research has to define which methods aremost suitable to obtain the best results in which situation—as alwaysthis also depends on personal preferences of the individual neurosur-geon. The authors have demonstrated that electrophysiological meth-ods, fibre tracking and intraoperative imaging can be combinedreliably. Intraoperative imaging allows compensating for the effectsof brain shift, so that even diffusion tensor imaging data can be updatedintraoperatively.

Mario Giordano, Hannover, GermanyA growing amount of evidence suggests that in the treatment of

cerebral gliomas the extent of resection correlates with patient’s sur-vival [1, 2]. Unfortunately location in close proximity to highly elo-quent cortical and subcortical structures is the main limiting factors forcomplete tumour removal. In this well-written paper, the authors pres-ent a short series of patients harbouring lesions that involve motorcortex and/or corticospinal tract surgically treated with the use ofintraoperative MRI and cortical/subcortical mapping. All the lesionshave been completely removed and despite the localization, the out-come of the patients is excellent.

This work is a good technical example of how the implementationof new technologies in neurosurgery allows performing safer and moreradical approaches. Moreover it emphasizes the importance to obtain amaximal tumour removal preserving patient’s quality of life.

References1. Keles GE, Lamborn KR, Berger MS: Low-grade hemispheric

gliomas in adults: a critical review of extent of resection as a factorinfluencing outcome. J Neurosurg. 2001;95(5):735–745.

2. Sanai N, Berger MS: Glioma extent of resection and its impact onpatient outcome. Neurosurgery. 2008;62(4):753–766.

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