Upload
others
View
0
Download
0
Embed Size (px)
Citation preview
Pearls and Pitfalls of MR Diffusion
in Clinical Neurology Dr. Alberto Bizzi Neuroradiology Unit Fondazione IRCCS Istituto Neurologico Carlo Besta Milan, Italy Email: [email protected]
Diffusion Tensor Imaging (DTI)(1) measures the effects of tissue
microstructure on the random walks (brownian motion) of water molecules in
the brain. In tissues with an orderly oriented microstructure, such as the
cerebral white matter, the measured diffusivity of water varies with the tissue’s
orientation (anisotropic diffusion). Water diffuses fastest along the principal
direction of the fibers, and slowest along the cross-‐sectional plane. The DTI
model provides the required information to construct a diffusion ellipsoid in
each voxel of an imaging volume. DTI measures the diffusivities of water
molecules along the three orthogonal axes of the ellipsoid (eigenvalues) and
their average (mean diffusivity). Fractional anisotropy is a measure of
eccentricity of the displacement of water molecules. In the healthy human brain
probably the most relevant factor affecting fractional anisotropy is the intravoxel
orientation coherence of white matter fibers(2).
There are three main imaging output of DTI MR imaging: quantitative
parametric maps displayed in gray scale (i.e. fractional anisotropy maps), color
maps showing the principal orientation of diffusion for each voxel and 3
dimensional maps showing virtual dissection of tracts with streamline tracking
methods.
In the interest of time in the oral presentation we’ll focus on diffusion
MR Tractography and its clinical application in brain tumors, stroke, multiple
sclerosis, prion disorders and neurodegenerative diseases (Alzheimer,
Amyotrophic Lateral Sclerosis). The aim of MR Tractography or fiber tracking is
to infer the three-‐dimensional trajectories of white matter bundles by piecing
together discrete estimates of the underlying continuous fiber orientation field
measured non-‐invasively with DTI data(3, 4).
Fiber tracking algorithms can be broadly classified into two types:
deterministic and probabilistic. Few DTI Tractography atlases for virtual in vivo
dissection of the principal human white matter tracts using a deterministic
approach have been recently published(5-‐7). Few limitations of fiber tracking
performed with the deterministic approach motivated the development of
probabilistic tracking algorithms(5). It is very important to understand well the
inherent limitations of all methods of DTI-‐based virtual dissections and
measurements. One important limitation is that in each voxel the eigen vector is
the average of the orientation of all bundles included in the voxel. In volumes of
white matter with many crossing bundles, as in the frontal and parietal
paraventricular white matter, fractional anisotropy is low and the degree of
uncertainty in the estimation of bundle orientation increases.
An attempt to overcome the limitation of crossing fibers has been addressed
with the development of more sophisticated imaging acquisition schemes using
high angular resolution diffusion imaging (HARDI)(6).
It is important to emphasize that, given the relative size differences
between the individual axons (1–5 micron) and voxels (2–3 mm) size, it is
possible to observe white matter anatomy only from a macroscopic point of view
with MR Tractography. Notwithstanding, the anatomic detail provided by MR
Tractography with 10-‐15 min of MR acquisition is unparalleled.
Encouraging results with DTI have been reported in several neurological
disorders: brain tumors, stroke, multiple sclerosis, amyotrophic lateral sclerosis,
Alzheimer disease and other dementias. In the interest of time we’ll focus on the
application that is probably closer to become of clinical use: diffusion MR
Tractography in presurgical planning.
The integration of functional data acquired with fMRI and MEG into the
navigational data sets has improved quick identification of eloquent cortex with
intraoperative ESM in the operating room. To avoid postoperative neurological
deficits, however, it is also necessary to preserve the white matter tracts
connecting eloquent cortex.
Diffusion MR Tractography has recently emerged as potentially valuable
clinical tool for presurgical planning(7-‐9) and intraoperative imaging-‐guided
navigation in the operating room(10). Diffusion MR Tractography can provide
the neurosurgeon with additional information about brain anatomy, pathology
and architecture that conventional MRI methods cannot.
Fig. 1 -‐ Directionally encoded color maps in a 65 years old male with glioblastoma multiforme in the left dorsolateral prefrontal region. The mass has infiltrated the superior longitudinal fasciculus, including the arcuate fasciculus (displayed in green, see cursor).
The directionally encoded color maps, with hues reflecting tensor
orientation and intensity weighted by fractional anisotropy, provides an
aesthetic and informative synthesis of tissue microstructure and architecture.
The color maps are a promising tool for delineation of tumor extent and
infiltration. DTI color maps indicate whether a mass is displacing, infiltrating or
destroying the main white matter tracts(11). MR Tractography can be used to
virtually dissect functionally critical white matter tracts, such as the
corticospinal tract and the arcuate fasciculus (AF), enabling the neurosurgeon to
identify and preserve the tract during resection(12).
It has been shown that acquisition of DTI color maps is feasible also in the
operating room with intraoperative 1.5 Tesla MR scanners. Intraoperative DTI
can depict shifting of major white matter tracts that may occur during surgical
removal of the mass. It has been shown that shifting of brain structures may be
unpredictable, therefore intraoperative updating of the navigation system is
strongly recommended(10).
Fig. 2 – Streamlines of the three segments of the left arcuate fasciculus (AF: long segment in red, anterior in green, posterior in yellow) are displied on the diffusion-‐weighted image at the level of a mass in the left posterior mesial temporal lobe. In this 70 years-‐old male with glioblastoma multiforme, MR Tractography was essential to demonstrate that the mass had not destroyed but only displaced the AF posteriorly and laterally. Streamlines of the AF confirmed that most of the fasciculus was intact.
Three dimensional objects of preoperative virtually dissected tracts can
be reliably integrated into a standard neuronavigation system, allowing for
intraoperative visualization and localization of the main tracts(13). MR
Tractography may show the relationship of the mass to the virtually dissected
AF. Virtual dissection of the three segments of the AF may show whether the
mass has partially interrupted or only displaced each of the three segments of
the AF. Display of MR Tractography results may also be useful in the operating
room when the neurosurgeon is approaching an important bundle and he wants
to reinforce his anatomical orientation in the operating field and consider
whether to use subcortical ESM to test the functional relevance of a specific
tract(14).
Fig. 3 – Streamlines of the left inferior frontal occipital fasciculus (IFOF) and fMRI (sentence comprehension task) are overlaid on FLAIR images, neuronavigator-‐ready for guiding surgery in the operating room. In this 62 years-‐old woman with fibrillary astrocytoma in the left temporal pole, MR Tractography demonstrated that the mass had partially interrupted the uncinate fasciculus (UF, not shown), while the IFOF (in pink) appears intact. Note the close relationship of the left IFOF with the hyperintense mass in the temporal pole.
Modern cognitive models of language have shown that there is a lot of
redundancy in the language network. It is of paramount importance to identify
those bundles that if severed may cause permanent language deficits. Definition
of which bundles are functionally eloquent and have to be absolutely spared
during resection remains an important issue.
There is a long list of important limitations(15). Few are inherent to the
DTI and the MR Tractography technology and they must be well understood
before the results of presurgical MR Tractography dissections can be safely
exported to the operating room. It is not yet established whether resection of
fibers apparently infiltrated by the tumor that appear to be interrupted or
destroyed on diffusion MR Tractography will result in permanent postoperative
neurologic deficits(15). Nevertheless, it should be established whether resection
of fibers that on MR Tractography appear to be interrupted within the tumor will
cause permanent postoperative deficits. On the contrary, it has been shown
many times that severing of the pyramidal tract will cause hemiplegia. Whether
severing of one of the many language connections will cause aphasia is currently
a controversial issue(16).
In conclusion, diffusion MR Tractography has emerged as a valuable tool
in the evaluation of motor and language pathways both in healthy individuals
and in patients with neurological disorders. In healthy subjects they are
contributing to refine current cognitive and anatomic models. Not only they have
confirmed several theories about language processing, but they have also raised
unexpected important questions. In patients with brain tumors they have
obtained recognition as valuable presurgical clinical tools in the determination of
hemispheric dominance and in the selection of candidates who may benefit from
awake craniotomy.
References 1. Basser PJ, Mattiello J, LeBihan D. MR diffusion tensor spectroscopy and imaging. Biophys
J 1994; 66:259-‐267. 2. Pierpaoli C, Jezzard P, Basser PJ, Barnett A, Di Chiro G. Diffusion tensor MR imaging of
the human brain. Radiology 1996; 201:637-‐648. 3. Conturo TE, Lori NF, Cull TS, et al. Tracking neuronal fiber pathways in the living human
brain. Proc Natl Acad Sci U S A 1999; 96:10422-‐10427. 4. Mori S, Crain BJ, Chacko VP, van Zijl PC. Three-‐dimensional tracking of axonal projections
in the brain by magnetic resonance imaging. Ann Neurol 1999; 45:265-‐269. 5. Jones DK. Studying connections in the living human brain with diffusion MRI. Cortex
2008; 44:936-‐952. 6. Seunarine KK, Alexander DC. Multiple Fibers: Beyond the Diffusion Tensor. In: Johansen-‐
Berg H, Behrens TE, eds. Diffusion MRI: From Quantitative Measurement to in Vivo Neuroanatomy. Oxford, U.K.: Elsevier, 2009; 55-‐72.
7. Clark CA, Barrick TR, Murphy MM, Bell BA. White matter fiber tracking in patients with space-‐occupying lesions of the brain: a new technique for neurosurgical planning? Neuroimage 2003; 20:1601-‐1608.
8. Field AS, Alexander AL, Wu YC, Hasan KM, Witwer B, Badie B. Diffusion tensor eigenvector directional color imaging patterns in the evaluation of cerebral white matter tracts altered by tumor. J Magn Reson Imaging 2004; 20:555-‐562.
9. Mori S, Frederiksen K, van Zijl PC, et al. Brain white matter anatomy of tumor patients evaluated with diffusion tensor imaging. Ann Neurol 2002; 51:377-‐380.
10. Nimsky C, Ganslandt O, Hastreiter P, et al. Intraoperative diffusion-‐tensor MR imaging: shifting of white matter tracts during neurosurgical procedures-‐-‐initial experience. Radiology 2005; 234:218-‐225.
11. 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; 25:356-‐369.
12. Laundre BJ, Jellison BJ, Badie B, Alexander AL, Field AS. Diffusion tensor imaging of the corticospinal tract before and after mass resection as correlated with clinical motor findings: preliminary data. AJNR Am J Neuroradiol 2005; 26:791-‐796.
13. Nimsky C, Ganslandt O, Fahlbusch R. Implementation of fiber tract navigation. Neurosurgery 2006; 58:ONS-‐292-‐304.
14. 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; 39:369-‐382.
15. Bizzi A. Presurgical Mapping of Verbal Language in Brain Tumors with Functional MR Imaging and MR Tractography. In: Pia Sundgren M, ed. Advanced Imaging Techniques in Brain Tumors: Elsevier, 2009; 573-‐596.
16. Bello L, Gallucci M, Fava M, et al. Intraoperative subcortical language tract mapping guides surgical removal of gliomas involving speech areas. Neurosurgery 2007; 60:67-‐82.