BOLD and DTI for Presurgical

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Nov 17, 2013 (3 years and 8 months ago)

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1

BOLD and DTI for
Presurgical

Mapping



Jay J.
Pillai
, M.D.

Director of Functional
MRI

Associate Professor

Neuroradiology

Division

The Russell H. Morgan Department of

Radiology and Radiological Science

Johns Hopkins Univ. School of Medicine

What is the purpose of
presurgical

mapping? Why fMRI & DTI?


Preop

risk assessment


Planning
surg

trajectory


Planning
intraop

mapping


Eloquent cortex & eloquent WM
---
goal of neurosurgery


Added value

patient interactive (H & P, training, education
prescan
), very different from volunteer research scanning

2

Typical Language Paradigms


Expressive Language Tasks


Verbal Fluency/Phonemic Fluency


Rhyming (Phonological)


Object Naming


Receptive Language Tasks


Sentence Comprehension (V/A)/Story Listening


Sentence Completion


Semantic Decision (category,
nva
, s/a)

3

Essential vs. Nonessential Activation


Complementary role of
intraop

mapping


Role of convergent activation


Role of statistical
thresholding

4

Typical Motor Paradigms


Hand Motor


Bilateral simultaneous or alternating R/L hand


AFT, hand clenching, thumb
-
index apposition


Foot Motor


Toe flexion/extension


Ankle flexion/extension


Face Motor


Tongue movement

lateral or vertical


Lip puckering


5

6



Classical
Brodmann’s

areas

From Waxman SG. Correlative
Neuroanatomy
, 24
th

Ed. Lange Medical Books/McGraw
-
Hill, New York, 2000.

7

Diffusion Tensor Imaging


Eloquent White Matter is just as important as Eloquent Cortex


Damage to eloquent white matter similar to resection of eloquent cortex



Water molecule diffusion is directionally dependent

anisotropy



The direction of maximum diffusivity coincides with the WM fiber
tract orientation


8

The Diffusion Tensor


The “diffusion
tensor”is

a matrix of numbers (mathematical model
describing diffusion in 3D space) derived from diffusion measurements in
several different directions (6+ directions for diffusion encoding).



This tensor depicted as
ellipsoid

whose orientation is described by three
eigenvectors

and its
shape

by three
eigenvalues
, which are its dimensions
(corresponding to diffusivity in each direction).
2





1,2

Jellison BJ, Field AS, Medow J, Lazar M, Salamat MS, Alexander AL.
Diffusion tensor imaging of cerebral white matter: a
pictorial review of physics, fiber tract anatomy, and tumor imaging patterns.

AJNR Am J Neuroradiol. 2004 Mar;25(3):356
-
69



9

Additional white matter tracts

sagittal

tractograms

Normal SLF

Adapted from
Brian J. Jellison, Aaron S. Field, Joshua Medow, Mariana Lazar, M. Shariar Salamat, and Andrew L. Alexander. Diffusion Tensor

Im
aging of Cerebral White Matter: A Pictorial
Review of Physics, Fiber Tract Anatomy, and Tumor Imaging Patterns.
AJNR Am. J. Neuroradiol.

2004; 25: 356
-

369.


Arcuate Fasciculus

important for
language
function/SLF

Superior
Fronto
-
Occipital
Fasciculus

Inferior
Fronto
-
Occipital
Fasciculus

Inferior
Longitudinal
Fasciculus

SLF


4 parts of SLF:


SLF I
-
--
horizontal fibers connecting superior parietal lobe to
frontal/
opercular

regions (
premotor

areas and SMA)


SLF II
-
--
horizontal fibers connecting the AG to posterior prefrontal
cortices


SLF III
-
--
horizontal fibers connecting the SMG to F lobe (pars
opercularis

/ventral
premotor

areas [BA 44] and ventral prefrontal area
[BA 46])


SLF IV
---
AF
-
--

connects STG/MTG to frontal regions (caudal dorsal
prefrontal cortex,
precentral

gyrus

but not BA as previously thought)

10

Bernal B, Altman N. The connectivity of the superior longitudinal fasciculus: a
tractography

DTI study. Magnetic
Resonance Imaging 28 (2010) 217

225.

Schmahmann

JD,
Pandya

DN, Wang R, Dai G,
Darceuil

HE, de
Crespigny

AJ,
Wedeen

VJ. Association
fibre

pathways of
the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 2007; 130:630
-
653.

11

Functions of the SLF components


SLF I
: higher order control of body
-
centered action based on
proprioception

and initiation of motor activity


SLFII
: involved in focusing spatial attention (hemi
-
inattention/neglect w
lesions)


SLF III
: involved in the gestural component of language and
orofacial

working memory (lesions result in cortical
dysarthria
, oral/
buccal

apraxias
,
impaired working memory)


SLF IV (AF):
thought that lesions result in conduction aphasia, but primate
evidence suggests that
ExC

and
MdLF

rather than AF responsible; AF
actually involved in spatial processing in the auditory domain (indicating
location and directionality of sounds rather than symbolic
repres

of
lang
)

12

Schmahmann

JD,
Pandya

DN, Wang R, Dai G,
Darceuil

HE, de
Crespigny

AJ,
Wedeen

VJ. Association
fibre

pathways of the brain: parallel observations from diffusion spectrum imaging and autoradiography.
Brain 2007; 130:630
-
653.

13

Martino J, De Witt
Hamer

PC, Berger MS, Lawton MT, Arnold CM, de Lucas EM,
Duffau

H. Analysis of the
subcomponents and cortical terminations of the
perisylvian

superior longitudinal fasciculus: a fiber dissection and
DTI
tractography

study. Brain
Struct

Funct
. 2012 Mar 16.

Functions of various other important eloquent
tracts


1)
SFOF

responsible for initiation and preparation of speech movements and
limbic aspects of speech


2)
IFOF

involved in language ventral stream (semantic network, distinct from
phonological network mediated by SLF)


3)
ILF

role in ventral visual stream (object recognition, discrimination and
memory including facial recognition

lesion>>>
prosopagnosia
)

actually lateral
to SS


4)
Uncinate

fasciculus


processing novel information, understanding emotional
aspects of sounds, regulation of emotional responses to auditory stimuli, enables
interaction between emotion and cognition, self
-
regulation, retrieval of past
information


5)
Cingulum

bundle

dorsal limbic pathway linking caudal
cingulate

gyrus

with
HC and PHG (memory), prefrontal areas 9 & 46 (manipulating info, monitoring
behavior, working memory)

critical for motivational and emotional aspects of
behavior, spatial working memory (
cingulotomy

for OCD)

14

Schmahmann

JD,
Pandya

DN, Wang R, Dai G,
Darceuil

HE, de
Crespigny

AJ,
Wedeen

VJ. Association
fibre

pathways of
the brain: parallel observations from diffusion spectrum imaging and autoradiography. Brain 2007; 130:630
-
653.

Aralasmak

A, Ulmer JL,
Kocak

M,
Salvan

CV, Hillis AE, Yousem DM. Association, Commissural and Projection Pathways
and Their Functional Deficit Reported in Literature. J
Comput

Assist
Tomogr

2006; 30:695
-
715.

15

DTT Validation:
Bello et al.
Neuroimage

2008



Study of 52 pts w LGG and 12 w HGG



There was a high correlation between DT
-
FT and
ISM
(sensitivity for CST=95%, language tracts=97%).




The combination of both methods decreased the duration of
surgery, patient fatigue, and
intraoperative

seizures.

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 Jan 1;39(1):369
-
82. Epub 2007 Aug 29

16

Limitations of DTT


4 different DTT software packages for display of CST of a single
normal subject; 3 used FACT (Fiber Assignment by Continuous
Tracking) method, one used
Tensorline

Propagation Algorithm.


None of the software applications was able to display the CST in its full
anatomical extent


The 4 packages did not lead to comparable tracking results despite use
of similar or identical tracking algorithms

Bürgel U
, Mädler B, Honey CR, Thron A, Gilsbach J, Coenen VA.Fiber tracking
with distinct software tools results in a clear diversity in anatomical fiber tract
portrayal.

Cen Eur Neurosurg. 2009 Feb;70(1):27
-
35.


Clinical Value of DTT vs. color directional
diffusion maps


DTT is excellent for isolating tracts that run alongside other parallel tracts


Major limitation for clinical use is
undersampling

of the tract
---
operator
-
dependent seeding, anatomic distortion.


FA/
angulation

thresholds, step sizes arbitrary


Error propagation

1
st

vs

2
nd

order processing


Numerous algorithms
---
deterministic (discrete,
subvoxel
) & probabilistic
DTT with very little validation


17

18

Validation of
fMRI
: studies comparing
fMRI

to Wada
and ECS results:


FROM: Pillai JJ, Language fMRI IN Holodny AI (Ed), Functional Neuroimaging: A Clinical Approach,
2008, Informa Healthcare (New York, NY)



2

Giussani
, Carlo; Roux, Frank
-
Emmanuel; MD, PhD;
Ojemann
, Jeffrey;
Sganzerla
, Erik;
Pirillo
, David;
Papagno
,
Costanza

Is
Preoperative Functional Magnetic Resonance Imaging Reliable for Language Areas Mapping in Brain Tumor Surgery? Review of Lang
uag
e Functional Magnetic
Resonance
Imaging

Neurosurgery. 66(1):113
-
120, January 2010
.

BOLD
validation:

Studies
comparing
preop

language
fMRI

to
ECS

Giussani

et
al.,
Neurosurgery

Jan 2010

20

Impact of
preop

fMRI

on surgical
planning:

Petrella et al., Radiology, Sept. 2006;240:793
-
802



Functional MRI performed on
39 consecutive patients with brain tumors
.



Change in neurosurgical treatment plans

(as a result of preoperative
fMRI
)
occurred in 19 patients (
P

< .05),

with a more aggressive approach
recommended after imaging in 18 patients.



Functional MR imaging resulted in
reduced surgical time

(estimated
reduction, 15

60 minutes) in 22 patients

who underwent surgery, a more
aggressive resection in six, and a smaller craniotomy in two.



In four patients,
sparing of patients from additional testing

(e.g., Wada)

because of the functional MRI result.


Petrella JR, Shah LM, Harris KM et al. Preoperative functional MR imaging localization of language and motor areas: Effect
on therapeutic decision making in patents with potentially resectable brain tumors.
Radiology.

2006;240:793
-
802

21

Impact of
preop

fMRI

on postoperative
clinical outcome


Roessler

et al. J
Neurol

Neurosurg

Psychiatry 2005



Twenty two patients with
gliomas

near motor cortex

evaluated with both
motor 3T
fMRI

and
intraoperative

motor cortex stimulation (MCS).



FMRI motor foci were successfully detected in all patients preoperatively,
whereas
MCS was possible in only
17 of 22 patients

(77.3%).

In those 17
patients
, 100% agreement was found between MCS and
fMRI

for localization
of primary motor cortex within 10 mm.




Mild to moderate transient neurological deterioration occurred in six patients,
and a severe
hemiparesis

in one. All patients recovered within 3 months

(31.8% transient, 0% permanent morbidity).


Roessler K, Donat M, Lanzenberger R, Novak K, Geissler A, Gartus A, Tahamtan AR, Milakara D, Czech T, Barth M, Knosp E, Beist
ein
er R. Evaluation
of preoperative high magnetic field motor functional MRI (3 Tesla) in glioma patients by navigated electrocortical stimulatio
n a
nd postoperative
outcome. J Neurol Neurosurg Psychiatry. 2005 Aug;76(8):1152
-
7


22

Impact of
preop

DTI on Postsurgical Clinical
Outcome

Wu JS et al.,
Neurosurgery

2007



Studied 238 pts

118 underwent DTI, 120 std 3D
struct

scans only for
neuronavigation
.



Postoperative motor deterioration

occurred in 32.8% of control cases,
compared to 15.3% of the study cases

(P < 0.001).



The
6
-
month
Karnofsky

Performance Scale score

of study cases was
significantly higher than that of control cases
, P < 0.001; greater difference
for HGG than LGG.



For 81 HGGs, the
median survival

of study cases was 21.2 months
compared with 14.0 months

of control cases (P = 0.048).




Wu JS, Zhou LF, Tang WJ, Mao Y, Hu J, Song YY, Hong XN, Du GH. 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 Nov;61(5):935
-
48; discussion 948
-
9

Preop

BOLD
fMRI

may serve as a prognostic
indicator

recent paper by Wood et al.,
AJNR 2011


74 patients
w primary or met tumor underwent
BOLD motor
mapping



77 patients

underwent
BOLD language
mapping



Motor (p<0.001) and
lang

(P=0.009)LAD
signif

a/w

pre or
postop

deficits



Pre and
postop

deficits, grade, tumor loc and LAD predicted mortality



Motor deficits increased linearly
as dist from tumor to PSMC decreased,
while
lang

deficits
incr

exponentially
as dist from tumor to
lang

areas
decr

below 1 cm.


23

Wood JM,
Kundu

B, Utter A, et al. Impact of Brain Tumor Location on Morbidity and Mortality: A Retrospective
Functional MR Imaging Study. AJNR Am J
Neuroradiol

2011; 32(8): 1420
-
5.

Clinical impact of BOLD
fMRI

relationship
between LAD and motor/
lang

deficits

L
inear relationship (
R
2
=0.99) between distance from the tumor to the area of activation and the existence of motor deficits (red)
and an asymptotic relationship (exponential fit,
R
2
=0.88) between the distance from the tumor to the area of activation and
the existence of language deficits
. Error bars depict 95% CIs calculated for a proportion.


24

Wood JM,
Kundu

B, Utter A, et al. Impact of Brain Tumor Location on Morbidity and Mortality: A Retrospective
Functional MR Imaging Study. AJNR Am J
Neuroradiol

2011; 32(8): 1420
-
5.