Revista Chilena de Neurocirugía 36 : 2011

Impact of the combined use of tractography, functional

magnetic resonance imaging and brain neuronavigation
on high grade glioma extent of resection
Impacto del uso combinado de la tractografía, resonancia magnética funcional y
la neuronavegación cerebral en el grado de resección de gliomas de alto grado

Ricardo.Prat*, Inmaculada Galeano*, Almudena Lucas **, Gaspar Reynes ***, Román Amador R****.

H. Universitario La Fe. Valencia. Campanar, 21, 46009 Valencia Spain, Group of Neurooncology. *Department of Neurosurgery.
** Department of MRI.
*** Department of Medical Oncology.
**** Department of Radiotherapy.

Rev. Chil. Neurocirugía 36: 40-45, 2011

Abstract
Introduction: Maximal surgical resection of brain high grade glioma, involves the risk of damaging either eloquent cortical areas
or efferent subcortical white matter tracts. Identification of the anatomical and functional relation between the tumor and adja-
cent functional cortical areas or eloquent white matter bundles may provide critical information to guide tumor resection and
prevent surgical morbidity. The main objective of this study was to assess the combined use of diffusion tensor (DT) tractography
and functional magnetic resonance (fMR) imaging to assist in the extent of resection of brain high grade glioma (HGG) with pre-
servation of eloquent areas. Material and methods: 42 consecutive patients harboring brain HGG underwent surgery with the
purpose of maximal resection. Patients were randomly divided in two groups: Group A (22 cases): control group, and group B
(20 cases), where surgery was performed with navigation and combined use of DT imaging and fMR imaging. Results: Extent of
resection in group A was 81.5% and 90.5% in group B (ANOVAs test p=0, 03). We did not observed differences in postoperative
neurological deficit and surgical time between both groups. Conclusion: The combined use of tractography, functional MRI and
neuronavigation may provide critical information to guide brain high grade glioma resection without increasing surgical morbidity
or surgical time.

Resumen
Introducción: La resección radical de los gliomas cerebrales de alto grado (GCAG) comporta el riesgo de afectación tanto de
áreas corticales elocuentes como de los tractos subcorticales de sustancia blanca. La identificación de la relación anatómica y
funcional entre el tumor y las áreas corticales o los tractos de sustancia blanca elocuentes, puede proporcionar una información
fundamental para guiar la resección quirúrgica y contribuir a reducir la morbilidad postquirúrgica. El principal objetivo del estu-
dio es el análisis del uso combinado de la tractografía y la resonancia magnética funcional (RMf) en el grado de resección de
gliomas cerebrales de alto grado con preservación de áreas elocuentes. Material y métodos: Presentamos 42 pacientes con
diagnóstico de GCAG y localización próxima a córtex motor o áreas del lenguaje, que fueron intervenidos quirúrgicamente con
el objetivo de llevar a cabo una resección radical de la lesión. Los pacientes se distribuyeron de forma aleatoria en 2 grupos: el
grupo A (22 pacientes) fue el grupo control y el grupo B (20 casos) fue también intervenido pero utilizando la neuronavegación y
el uso combinado de tractografía y RMf. Resultados: El grado de resección en el grupo A fue de un 81,5% y del 90,5 en el grupo
B (test de ANOVA p=0,03). No observamos diferencias en la incidencia de morbilidad postquirúrgica o del tiempo de cirugía
entre ambos grupos. Conclusiones: El uso combinado de la tractografía, RMf y neuronavegación proporciona una información
funcional que facilita la cirugía de los GCAG sin incrementar la morbilidad o el tiempo de cirugía.

Keywords: Diffusion tensor; functional magnetic resonance; high grade glioma; neuronavigation; surgery; tractography.

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Trabajo Original Revista Chilena de Neurocirugía 36 : 2011

Introduction
Management of brain high grade glioma
depends on a multidisciplinary treatment
that includes surgery, radiotherapy and
chemotherapy. Although is a pathology
not curable with neurosurgical procedu-
res, the extent of resection might have
an influence on the further course of the
disease. Nevertheless, maximal surgical
resection of brain high grade glioma, in-
volves the risk of damaging either elo-
quent cortical areas or efferent subcor-
tical white matter tracts.
Diffusion tensor (DT) tractography is a
noninvasive magnetic resonance (MR)
technique that can provide subcortical
localization of motor pathways, whereas
functional magnetic resonance (fMR)
imaging has been proved to be useful in
the localization of eloquent cerebral cor-
tex. These techniques are complimen-
tary and allow both the identification of
the eloquent areas of the brain, and the
connections between them.
Identification of the anatomical and functio-
nal relation between the tumor and adja-
cent functional cortical areas or eloquent
white matter bundles may provide critical
information to guide tumor resection and
prevent surgical morbidity.
resection, being excluded brain biop-
sies. Patients were randomly divided in
two groups: Group A (22 cases): control
group, surgery with navigation without
combined use of DT imaging and fMR
imaging, and group B (20 cases), sur-
gery with navigation and combined use
of DT imaging and fMR imaging. Data
sets of DT imaging, magnetic resonance
imaging, and functional magnetic reso-
nance imaging were acquired preope-
ratively during the same investigation in
22 patients harboring brain high grade
glioma. Off-line processing of DT ima-
ging data was performed to visualize the
corticospinal tract (CST), superior longi-
tudinal tract, corpus callosum fibers and
uncinatus fascicule. The target region of
interest for the CST was placed in the
cerebral peduncle of the midbrain, whe-
re a high density of fibers of the descen-
ding motor pathway is found. fMR ima-
ging cortical activation maps of motor
and somatosensory regional activation
were obtained. Then this information
was transferred to the neuronavigation
system (Brainlab) to initiate functional
neuronavigation. (Fig.1)
A control MRI was performed not later
than 48h after surgery. The extent of re-
section observed in these control MRI
was assessed by regular team of neu-
roradiologists of our hospital and by an
external independent neuroradiologist.
As well as extent of resection, data sets
of age and sex, tumoral volume, tumoral
localization, surgical postoperative neu-
rological deficit and surgical time were
recorded. Univariate and multivariate
analysis were performed and a level of
signification < 0, 05 was established
to determine differences between both
groups in terms of extent of resection,
postoperative neurological deficit, and
surgical time.
Results
Twenty-two patients, 19 male and 3 fe-
male, formed the control group in which
the mean age was 59.9 years old with a
minimum of 28 and a maximum of 79. In
the studied group of twenty patients, 15
male and 5 female, the mean age was

This functional neuronavigation allows

the preoperative planning of patients
with mass lesions affecting functiona-
lly important brain regions as well as
to visualize intraoperatively eloquent
white matter bundles or gray matter
tissue with relationship to brain tumor.
The main objective of this study was
to assess the combined use of DT and
fMR imaging to assist in the increase of
resection of high grade glioma with im-
proved preservation of eloquent regions
during surgery.

Materials and Methods

Figure 1: Image of fusion of magnetic resonance imaging and tractography in

42 consecutive patients operated of high
a patient harbouring a right frontal high grade glioma.
grade glioma in two years were inclu-
ded in the study. All of them underwent
surgery with the purpose of maximal

41
 Revista Chilena de Neurocirugía 36 : 2011
57.9 with a minimum of 22 and a maxi-
mum of 78 years old.
In group A 14 patients out of 20 harbo-
red tumor in eloquent areas, whereas
in group B were 14 patients out of 22.
Pathology showed 18 glioblastoma mul-
tiform (GBM) and 4 anaplastic astro-
cytoma (AA) in group A and 15 GBM,
4 AA and 1 anaplastic ependymoma in
group B.
Tumoral volume in group A was less
than 20cc in 8 patients, from 20 to 40
cc in 7 patients and superior to 40 cc in
7 patients. In group B we found tumo-
ral volume less than 20cc in 8 patients,
from 20 to 40 cc in 6 patients and supe-
rior to 40 cc in 6 patients.
The extent of resection in group A was
60-70% in 4 patients, 70-80% in 5 pa-
tients, 80-90% in 1 patient and 90-
100% in 12 patients. In group B 60-70%
of resection was achieved in 2 patients,
70-80% in 2 patients, and 90-100% in
16 patients.
Overall the extent of resection in group A
was 81, 5% and 90, 5% in group B (ANO-
VAs test p=0, 03). In a multivariate analy-
sis, sex, age, pathology or tumoral volume
were found not to affect the different ex-
tent of resection between both groups.
Despite not being statistically signifi-
cant, we found a trend of a higher extent
of resection in eloquent areas in group B
(87.3% compared to 79.1% in group A).
In non eloquent areas a significant in-
crease of resection was found in group
B (100%) compared to group A (85.2%)
(ANOVAs test p=0,017). Resections ob-
served in eloquent areas in patients of
group B were superior to those obtai-
ned in non eloquent areas in group A.
We did not observed differences in
terms of postoperative neurological
morbidity between both groups (around
10% of patients), but those patients wi-
thout neurological complications belon-
ging to group B had a significant higher
extent of resection that those of group
42
A. (ANOVAs test p=0, 01). Surgical time
was found to have no differences bet-
ween groups.
Discussion
Preoperative assessment provided by
DT tractography and fMR about the
location of functional fiber tracts and
expressive cortical areas in patients
with brain tumor, cannot be obtained
by conventional imaging methods. Ne-
vertheless, knowledge of those critical
areas and their relationship to the tumor
is of major interest for reducing operati-
ve morbidity [19,33].
Accuracy of DTI and fMR
To establish the accuracy of both techni-
ques is of great value in order to rely on
the information provided to take intrao-
perative surgical decisions. In that way,
several studies have addressed this
problem verifying the estimated course
of a specific tract after direct intraope-
rative subcortical stimulation. The mean
distance between the stimulation sites
and the DT-imaged fiber tracks varies
from 2mm to 1cm in the pyramidal tract
[3,16,18,24] and to visualize language-
related subcortical connections, such
as the arcuate fasciculus (AF) distances
between the stimulus points and the AF
were within 6 mm [10]. In these studies
motor evoked potential (MEP) response
has been documented to be consis-
tently absent at distances beyond 10 to
13 mm of the estimated pyramidal tract
[11,18].
Intraoperative diffusion-weighted ima-
ging using an intraoperative MR scanner
of low magnetic field strength (0.3 Tesla)
has been developed demonstrating cli-
nical usefulness and efficacy in detec-
ting the pyramidal tract and its relations-
hip with tumor borders [26]. Comparing
with other techniques, DT tractogra-
phy appears to be more accurate than
functional magnetic resonance imaging
and somatosensory evoked magnetic
fields in detecting primary motor area,
with rates of successful detection bet-
ween 92 to 100% [5,12]. Several series
conclude that tractography imaging is
consistent with anatomical and functio-
nal intraoperative references and is use-
ful in neurological surgery. [2,4]
Several studies have focused on the
functional accuracy of fMR imaging
findings, evaluating the correlation bet-
ween fMR findings and the results of
intraoperative direct cortical stimulation
in patients who harbor tumors in elo-
quent areas. Correlation is high, from
82 to100% in different series, mainly in
the evaluation of motor function [8,9,27].
Nevertheless, in language cortical areas,
brain mapping additional to fMR is advi-
sed to make surgical decisions [30].
Limitations of the technique
Major limitations of the combined use of
DT tractography and fMR in the resec-
tion of HGG include a possible shifting
of the tracts after major tumor parts are
removed, the acquisition technique that
usually relies on subjective identification
of anatomical landmarks of a tract of
interest and the length of time required
for the procedure [1,6,22,23,24,31,39].
Shifted positions of the brain structures
after tumor removal have been compen-
sated usually with intraoperative upda-
tes by using motor evoked potentials
with intraoperative fiber stimulation [11],
intraoperative high-field magnetic reso-
nance imaging [20,23] including intrao-
perative tractography [22] and intrao-
perative three-dimensional ultrasound
neuronavigation system [7]. In some
cases it has been observed that the
images of fiber-tracking technique failed
to present the disposition of the fiber
bundles [1,13] due to the acquisition te-
chnique or vicinity of areas with elevated
water content (edema), tissue compres-
sion or fiber degeneration [31]. To avoid
fiber distortion it has been proposed to
use the seed region of interest for DT
tractography based on fMR, instead of
anatomical landmarks [31] and to apply
Trabajo Original
an automated approach of tract recons-
truction to reduce potential subjective
variability due to manual procedure [39].
As regards to the length of time required
for the procedure in our experience is
not significantly increased and has been
quantified to amount to up to 10 minutes
of added time. [21]
Clinical and operative results
Only one prospective, randomized con-
trolled study has been carried out in pa-
tients with cerebral glioma to study the
effect of tractography over the extent
of resection, postoperative morbidity
and Karnofsky Performance Scale, and
mean survival time [38].
Compared to the control group, the use
of DT tractography associated increa-
sed extent of resection in HGG (gross
total resection of 74.4 versus 33.3%
in control group), significantly higher
6-month Karnofsky Performance Scale
score and significantly lower postopera-
tive motor deterioration. Mean survival
after surgery in HGG was also signifi-
cantly longer.
Different studies have focused on the
safety of the tractography guided sur-
gery of tumors near the motor tract,
based on lower postoperative morbidity
mainly when associated with intraope-
rative brain stimulation [2,11,16,17,18,25]
. Preoperative planning by using com-
bination of fMR and DT tractography
appears to improve surgical results in
terms of function preservation [9]. Ne-
vertheless, the increase of the extent of
resection due to that preoperative com-
bination has been infrequently addres-
sed with only 27% of complete resec-
tions being reported. These data were
improved by using intraoperative MRI up
to 40% of patients with complete resec-
tions. Despite extended resections the
low postoperative morbidity remained
being frequently transient deficits [20].
More frequently, experiences with fMR
guided neuronavigation have been re-
ported with gross total resection(more
than 95%) of gliomas in 83% to 91% of
the patients and postoperative neurolo-
gical deterioration in 16% to 31% of pa-
tients [15,29].
It has been demonstrated in DT trac-
Revista Chilena de Neurocirugía 36 : 2011
tography studies that despite tumor of functional white matter fibers and en-
infiltration, swelling, apparent necrosis, sures higher extent of resection during
and gross distortion, anatomically intact surgery of high grade glioma.
fibers may remain located inside the tu- Three dimensional visualization of the
mor mass [2,14,32,34,35,36,37] . This white matter fibers such as corticos-
fact implies a modification of the surgi- pinal tract, optic radiation and arcuate
cal strategy in terms of avoiding posto- fasciculus with relationship to high gra-
perative neurological deterioration. An de gliomas is helpful, and when used
interesting experience has focused of routinely in neuronavigation surgery of
the impact of tractography on the surgi- high grade glioma does not increase the
cal procedure in terms of modification of length of surgery neither increase the
surgical approach and extent of resec- neurological deficit rate despite the in-
tion during surgery and has quantified it creased resection in both eloquent and
to appear in 80% of cases [28]. non eloquent areas.
Our results in terms of extent of resec- The main drawbacks of the technique
tion are consistent with those of the lite- are the intraoperative shift of the tracts
rature. Even though our series include after tumor removal and the subjective
patients harboring tumor in presumably procedure of selection of fiber tracts du-
non eloquent areas, the extent of resec- ring the acquisition of DT tractography
tion of 87.3% in eloquent areas compa-
res favorably with those of the majority Recibido: 25.09.10
of larger series, mainly given the fact Aceptado:13.10.10
that no intraoperative method was used
to correct brain shift or verify eloquent
cortical or white matter areas. The only
prospective, randomized controlled stu-
dy performed to assess the usefulness
of tractography in surgical resection
of gliomas found a significantly clini-
cal improvement in terms of Karnofsky
performance scale, neurological deficit
and survival [38]. Our study does not
include survival analysis, but patients
of the studied group did not differ from
those of the control group in number of
postoperative neurological deficit. With
regard to this fact, it should be taken
into consideration the higher rate of mo-
tor deterioration observed 32.8% in the
control group of the randomized contro-
lled study compared to 10% detected in
the present study. Even though we did
not reduce the rate of neurological dete-
rioration, we significantly increased the
extent of resection in patients without
neurological postoperative complica-
tions.
Conclusions
The combination of fMRI with DT trac-
tography allows for assessment of elo-
quent cerebral cortex and visualization
43
 Revista Chilena de Neurocirugía 36 : 2011

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Corresponding author:
Ricardo Prat
Address: Paseo Alameda, 64-10º-pta 47, 46023 Valencia (Spain)
Phone: 01134609781016. Fax: 01134963866769
e-mail: ricprat@ono.com

Trabajo presentado de forma preliminar en el Congreso de la Sociedad Española de Neurocirugía celebrado en Valencia en 2008.

45